Skip to main content

Advertisement

Log in

Pathological mechanisms of cold and mechanical stress in modulating cancer progression

  • Review Article
  • Published:
Human Cell Aims and scope Submit manuscript

Abstract

Environmental temperature and cellular mechanical force are the inherent factors that participate in various biological processes and regulate cancer progress, which have been hot topics worldwide. They occupy a dominant part in the cancer tissues through different approaches. However, extensive investigation regarding pathological mechanisms in the carcinogenic field. After research, we found cold stress via two means to manipulate tumors: neuroscience and mechanically sensitive ion channels (MICHs) such as TRP families to regulate the physiological and pathological activities. Excessive cold stimulation mediated neuroscience acting on every cancer stage through the hypothalamus-pituitary-adrenocorticoid (HPA) to reach the target organs. Comparatively speaking, mechanical force via Piezo of MICHs controls cancer development. The progression of cancer depends on the internal activation of proto-oncogenes and the external tumorigenic factors; the above two means eventually lead to genetic disorders at the molecular level. This review summarizes the interaction of bidirectional communication between them and the tumor. It covers the main processes from cytoplasm to nucleus related to metastasis cascade and tumor immune escape.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Availability of data and materials

The datasets used and analyzed during the current study are available from the corresponding author upon reasonable request.

References

  1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100(1):57–70.

    Article  CAS  PubMed  Google Scholar 

  2. Lengauer C, Kinzler KW, Vogelstein B. Genetic instabilities in human cancers. Nature. 1998;396(6712):643–9.

    Article  CAS  PubMed  Google Scholar 

  3. Calle EE, Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer. 2004;4(8):579–91.

    Article  CAS  PubMed  Google Scholar 

  4. Nikolaev YA, Cox CD, Ridone P, Rohde PR, Cordero-Morales JF, Vásquez V, et al. Mammalian TRP ion channels are insensitive to membrane stretch. J Cell Sci. 2019. https://doi.org/10.1242/jcs.238360.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Voskarides K. The, “cancer-cold” hypothesis and possible extensions for the Nordic populations. Scandinavian J Public Health. 2019;47(5):477–81.

    Article  Google Scholar 

  6. Sharma A, Verma HK, Joshi S, Panwar MS, Mandal CC. A link between cold environment and cancer. Tumour Biol. 2015;36(8):5953–64.

    Article  CAS  PubMed  Google Scholar 

  7. Chatra K, Kuppili V, Edla DR, Verma AK. Cancer data classification using binary bat optimization and extreme learning machine with a novel fitness function. Med Biol Eng Comput. 2019;57(12):2673–82.

    Article  PubMed  Google Scholar 

  8. Wang Y, Guan J, Wang H, Wang Y, Leeper D, Iliakis G. Regulation of dna replication after heat shock by replication protein a-nucleolin interactions. J Biol Chem. 2001;276(23):20579–88.

    Article  CAS  PubMed  Google Scholar 

  9. Estrada LD, Ağaç D, Farrar JD. Sympathetic neural signaling via the β2-adrenergic receptor suppresses T-cell receptor-mediated human and mouse CD8(+) T-cell effector function. Eur J Immunol. 2016;46(8):1948–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Bucsek MJ, Giridharan T, MacDonald CR, Hylander BL, Repasky EA. An overview of the role of sympathetic regulation of immune responses in infectious disease and autoimmunity. Int J Hypertherm. 2018;34(2):135–43.

    Article  CAS  Google Scholar 

  11. Robinson EL, Bagchi RA, Major JL, Bergman BC, Matsuda JL, McKinsey TA. HDAC11 inhibition triggers bimodal thermogenic pathways to circumvent adipocyte catecholamine resistance. J Clin Investig. 2023. https://doi.org/10.1172/JCI168192.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Jin J, Miao C, Wang Z, Zhang W, Zhang X, Xie X, et al. Design and synthesis of aryloxypropanolamine as β(3)-adrenergic receptor antagonist in cancer and lipolysis. Eur J Med Chem. 2018;150:757–70.

    Article  CAS  PubMed  Google Scholar 

  13. Sereni F, Dal Monte M, Filippi L, Bagnoli P. Role of host β1- and β2-adrenergic receptors in a murine model of B16 melanoma: functional involvement of β3-adrenergic receptors. Naunyn Schmiedebergs Arch Pharmacol. 2015;388(12):1317–31.

    Article  CAS  PubMed  Google Scholar 

  14. Bellinger DL, Lorton D. Autonomic regulation of cellular immune function. Auton Neurosci. 2014;182:15–41.

    Article  CAS  PubMed  Google Scholar 

  15. Cohen S, Levi-Montalcini R, Hamburger V. A nerve growth-stimulating factor isolated from Sarcom as 37 and 180. Proc Natl Acad Sci USA. 1954;40(10):1014–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Heitz F, Hengsbach A, Harter P, Traut A, Ataseven B, Schneider S, et al. Intake of selective beta blockers has no impact on survival in patients with epithelial ovarian cancer. Gynecol Oncol. 2017;144(1):181–6.

    Article  CAS  PubMed  Google Scholar 

  17. Barron TI, Connolly RM, Sharp L, Bennett K, Visvanathan K. Beta blockers and breast cancer mortality: a population- based study. J Clin Oncol. 2011;29(19):2635–44.

    Article  CAS  PubMed  Google Scholar 

  18. Melhem-Bertrandt A, Chavez-Macgregor M, Lei X, Brown EN, Lee RT, Meric-Bernstam F, et al. Beta-blocker use is associated with improved relapse-free survival in patients with triple-negative breast cancer. J Clin Oncol. 2011;29(19):2645–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Wang HM, Liao ZX, Komaki R, Welsh JW, O’Reilly MS, Chang JY, et al. Improved survival outcomes with the incidental use of beta-blockers among patients with non-small-cell lung cancer treated with definitive radiation therapy. Annal Oncol. 2013;24(5):1312–9.

    Article  CAS  Google Scholar 

  20. Lee KW, Tsai YS, Chiang FY, Huang JL, Ho KY, Yang YH, et al. Lower ataxia telangiectasia mutated (ATM) mRNA expression is correlated with poor outcome of laryngeal and pharyngeal cancer patients. Annal Oncol. 2011;22(5):1088–93.

    Article  Google Scholar 

  21. Ghanemi M, Pourshohod A, Ghaffari MA, Kheirollah A, Amin M, Zeinali M, et al. Specific Targeting of HER2-Positive Head and Neck Squamous Cell Carcinoma Line HN5 by Idarubicin-ZHER2 Affibody Conjugate. Curr Cancer Drug Targets. 2019;19(1):65–73.

    Article  CAS  PubMed  Google Scholar 

  22. Huang Z, Li G, Zhang Z, Gu R, Wang W, Lai X, et al. β2AR-HIF-1α-CXCL12 signaling of osteoblasts activated by isoproterenol promotes migration and invasion of prostate cancer cells. BMC Cancer. 2019;19(1):1142.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Eng JW, Reed CB, Kokolus KM, Pitoniak R, Utley A, Bucsek MJ, et al. Housing temperature-induced stress drives therapeutic resistance in murine tumour models through β2-adrenergic receptor activation. Nat Commun. 2015;6:6426.

    Article  CAS  PubMed  Google Scholar 

  24. Al-Astal HI, Massad M, AlMatar M, Ekal H. Cellular functions of RNA-binding Motif protein 3 (RBM3): clues in hypothermia, cancer biology and apoptosis. Protein Pept Lett. 2016;23(9):828–35.

    Article  CAS  PubMed  Google Scholar 

  25. Bandyopadhayaya S, Ford B, Mandal CC. Cold-hearted: a case for cold stress in cancer risk. J Therm Biol. 2020;91: 102608.

    Article  CAS  PubMed  Google Scholar 

  26. Hirata K, Nagasaka T. Enhancement of calorigenic response to cold and to norepinephrine in physically trained rats. Jpn J Physiol. 1981;31(5):657–65.

    Article  CAS  PubMed  Google Scholar 

  27. Afsarian O, Shahir MH, Lourens A, Akhlaghi A, Lotfolahian H, Hoseini A, et al. Eggshell temperature manipulations during incubation and in ovo injection of thyroxine are associated with a decreased incidence of cold-induced ascites in broiler chickens. Poult Sci. 2018;97(1):328–36.

    Article  CAS  PubMed  Google Scholar 

  28. Shmakov DN, Nuzhny VP, Kibler NA, Kharin SN. Changes in total cholesterol and heart rate in normotensive and hypertensive rats under combined influence of cold exposure and hypokinesia. Bull Exp Biol Med. 2020;169(6):738–41.

    Article  CAS  PubMed  Google Scholar 

  29. Zareei E, Karami F, Gholami M, Ershadi A, Avestan S, Aryal R, et al. Physiological and biochemical responses of strawberry crown and leaf tissues to freezing stress. BMC Plant Biol. 2021;21(1):532.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Shi H, Tan SJ, Zhong H, Hu W, Levine A, Xiao CJ, et al. Winter temperature and UV are tightly linked to genetic changes in the p53 tumor suppressor pathway in Eastern Asia. Am J Hum Genet. 2009;84(4):534–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. So CL, Milevskiy MJG, Monteith GR. Transient receptor potential cation channel subfamily V and breast cancer. Labor Investig. 2020;100(2):199–206.

    Article  CAS  Google Scholar 

  32. Wang Y, Yin S, Mei L, Yang Y, Xu S, He X, et al. A dual receptors-targeting and size-switchable “cluster bomb” co-loading chemotherapeutic and transient receptor potential ankyrin 1 (TRPA-1) inhibitor for treatment of triple negative breast cancer. J Controll Release. 2020;321:71–83.

    Article  CAS  Google Scholar 

  33. Zhan C, Shi Y. TRPC channels and cell proliferation. Adv Exp Med Biol. 2017;976:149–55.

    Article  CAS  PubMed  Google Scholar 

  34. Lin R, Bao X, Wang H, Zhu S, Liu Z, Chen Q, et al. TRPM2 promotes pancreatic cancer by PKC/MAPK pathway. Cell Death Dis. 2021;12(6):585.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Santoni G, Farfariello V. TRP channels and cancer: new targets for diagnosis and chemotherapy. Endocr Metab Immune Disord Drug Targets. 2011;11(1):54–67.

    Article  CAS  PubMed  Google Scholar 

  36. Kärki T, Tojkander S. TRPV protein family-from mechanosensing to cancer invasion. Biomolecules. 2021;11(7):1019.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Chen J, Luan Y, Yu R, Zhang Z, Zhang J, Wang W. Transient receptor potential (TRP) channels, promising potential diagnostic and therapeutic tools for cancer. Biosci Trends. 2014;8(1):1–10.

    Article  PubMed  Google Scholar 

  38. Su KH, Lin SJ, Wei J, Lee KI, Zhao JF, Shyue SK, et al. The essential role of transient receptor potential vanilloid 1 in simvastatin-induced activation of endothelial nitric oxide synthase and angiogenesis. Acta Physiol (Oxf). 2014;212(3):191–204.

    Article  CAS  PubMed  Google Scholar 

  39. Wong KK, Banham AH, Yaacob NS, Nur Husna SM. The oncogenic roles of TRPM ion channels in cancer. J Cell Physiol. 2019. https://doi.org/10.1002/jcp.28168.

    Article  PubMed  Google Scholar 

  40. Grolez GP, Chinigò G, Barras A, Hammadi M, Noyer L, Kondratska K, et al. TRPM8 as an anti-tumoral target in prostate cancer growth and metastasis dissemination. Int J Mol Sci. 2022;23(12):6672.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Anderson KJ, Cormier RT, Scott PM. Role of ion channels in gastrointestinal cancer. World J Gastroenterol. 2019;25(38):5732–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Lan X, Zhao J, Song C, Yuan Q, Liu X. TRPM8 facilitates proliferation and immune evasion of esophageal cancer cells. 2019. Biosci Rep. https://doi.org/10.1042/BSR20191878.

  43. Yee NS. TRPM8 ion channels as potential cancer biomarker and target in pancreatic cancer. Adv Protein Chem Struct Biol. 2016;104:127–55.

    Article  CAS  PubMed  Google Scholar 

  44. Lunardi A, Barbareschi M, Carbone FG, Morelli L, Brunelli M, Fortuna N, et al. TRPM8 protein expression in hormone naïve local and lymph node metastatic prostate cancer. Pathologica. 2021;113(2):95–101.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Gkika D, Lemonnier L, Shapovalov G, Gordienko D, Poux C, Bernardini M, et al. TRP channel-associated factors are a novel protein family that regulates TRPM8 trafficking and activity. J Cell Biol. 2015;208(1):89–107.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Zhang L, Barritt GJ. Evidence that TRPM8 is an androgen-dependent Ca2+ channel required for the survival of prostate cancer cells. Can Res. 2004;64(22):8365–73.

    Article  CAS  Google Scholar 

  47. Bidaux G, Roudbaraki M, Merle C, Crépin A, Delcourt P, Slomianny C, et al. Evidence for specific TRPM8 expression in human prostate secretory epithelial cells: functional androgen receptor requirement. Endocr Relat Cancer. 2005;12(2):367–82.

    Article  CAS  PubMed  Google Scholar 

  48. Thebault S, Lemonnier L, Bidaux G, Flourakis M, Bavencoffe A, Gordienko D, et al. Novel role of cold/menthol-sensitive transient receptor potential melastatine family member 8 (TRPM8) in the activation of store-operated channels in LNCaP human prostate cancer epithelial cells. J Biol Chem. 2005;280(47):39423–35.

    Article  CAS  PubMed  Google Scholar 

  49. Bidaux G, Flourakis M, Thebault S, Zholos A, Beck B, Gkika D, et al. Prostate cell differentiation status determines transient receptor potential melastatin member 8 channel subcellular localization and function. J Clin Investig. 2007;117(6):1647–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Tsavaler L, Shapero MH, Morkowski S, Laus R. Trp-p8, a novel prostate-specific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Can Res. 2001;61(9):3760–9.

    CAS  Google Scholar 

  51. Fuessel S, Sickert D, Meye A, Klenk U, Schmidt U, Schmitz M, et al. Multiple tumor marker analyses (PSA, hK2, PSCA, trp-p8) in primary prostate cancers using quantitative RT-PCR. Int J Oncol. 2003;23(1):221–8.

    CAS  PubMed  Google Scholar 

  52. Yee NS, Zhou W, Lee M. Transient receptor potential channel TRPM8 is over-expressed and required for cellular proliferation in pancreatic adenocarcinoma. Cancer Lett. 2010;297(1):49–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Yee NS, Li Q, Kazi AA, Yang Z, Berg A, Yee RK. Aberrantly over-expressed TRPM8 channels in pancreatic adenocarcinoma: correlation with tumor size/stage and requirement for cancer cells invasion. Cells. 2014;3(2):500–16.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Cucu D, Chiritoiu G, Petrescu S, Babes A, Stanica L, Duda DG, et al. Characterization of functional transient receptor potential melastatin 8 channels in human pancreatic ductal adenocarcinoma cells. Pancreas. 2014;43(5):795–800.

    Article  CAS  PubMed  Google Scholar 

  55. Yee NS, Chan AS, Yee JD, Yee RK. TRPM7 and TRPM8 ion channels in pancreatic adenocarcinoma: potential roles as cancer biomarkers and targets. Scientifica. 2012;2012: 415158.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Chodon D, Guilbert A, Dhennin-Duthille I, Gautier M, Telliez MS, Sevestre H, et al. Estrogen regulation of TRPM8 expression in breast cancer cells. BMC Cancer. 2010;10:212.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Liu J, Chen Y, Shuai S, Ding D, Li R, Luo R. TRPM8 promotes aggressiveness of breast cancer cells by regulating EMT via activating AKT/GSK-3β pathway. Tumour Biol. 2014;35(9):8969–77.

    Article  CAS  PubMed  Google Scholar 

  58. Du GJ, Li JH, Liu WJ, Liu YH, Zhao B, Li HR, et al. The combination of TRPM8 and TRPA1 expression causes an invasive phenotype in lung cancer. Tumour Biol. 2014;35(2):1251–61.

    Article  CAS  PubMed  Google Scholar 

  59. Wang Y, Yang Z, Meng Z, Cao H, Zhu G, Liu T, et al. Knockdown of TRPM8 suppresses cancer malignancy and enhances epirubicin-induced apoptosis in human osteosarcoma cells. Int J Biol Sci. 2013;10(1):90–102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Okamoto Y, Ohkubo T, Ikebe T, Yamazaki J. Blockade of TRPM8 activity reduces the invasion potential of oral squamous carcinoma cell lines. Int J Oncol. 2012;40(5):1431–40.

    CAS  PubMed  Google Scholar 

  61. Louhivuori LM, Bart G, Larsson KP, Louhivuori V, Näsman J, Nordström T, et al. Differentiation dependent expression of TRPA1 and TRPM8 channels in IMR-32 human neuroblastoma cells. J Cell Physiol. 2009;221(1):67–74.

    Article  CAS  PubMed  Google Scholar 

  62. Wondergem R, Bartley JW. Menthol increases human glioblastoma intracellular Ca2+, BK channel activity and cell migration. J Biomed Sci. 2009;16(1):90.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Mergler S, Strowski MZ, Kaiser S, Plath T, Giesecke Y, Neumann M, et al. Transient receptor potential channel TRPM8 agonists stimulate calcium influx and neurotensin secretion in neuroendocrine tumor cells. Neuroendocrinology. 2007;85(2):81–92.

    Article  CAS  PubMed  Google Scholar 

  64. Koike C, Obara T, Uriu Y, Numata T, Sanuki R, Miyata K, et al. TRPM1 is a component of the retinal ON bipolar cell transduction channel in the mGluR6 cascade. Proc Natl Acad Sci USA. 2010;107(1):332–7.

    Article  CAS  PubMed  Google Scholar 

  65. Chinigò G, Fiorio Pla A, Gkika D. TRP channels and small GTPases interplay in the main hallmarks of metastatic cancer. Front Pharmacol. 2020;11: 581455.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Kolisek M, Beck A, Fleig A, Penner R. Cyclic ADP-ribose and hydrogen peroxide synergize with ADP-ribose in the activation of TRPM2 channels. Mol Cell. 2005;18(1):61–9.

    Article  CAS  PubMed  Google Scholar 

  67. Liao M, Cao E, Julius D, Cheng Y. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature. 2013;504(7478):107–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Kim M, Sisco NJ, Hilton JK, Montano CM, Castro MA, Cherry BR, et al. Evidence that the TRPV1 S1–S4 membrane domain contributes to thermosensing. Nat Commun. 2020;11(1):4169.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Doñate-Macián P, Álvarez-Marimon E, Sepulcre F, Vázquez-Ibar JL, Perálvarez-Marín A. The membrane proximal domain of TRPV1 and TRPV2 channels mediates protein_protein interactions and lipid binding in vitro. Int J Mol Sci. 2019;20(3):682.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Ramer R, Hinz B. Inhibition of cancer cell invasion by cannabinoids via increased expression of tissue inhibitor of matrix metalloproteinases-1. J Natl Cancer Inst. 2008;100(1):59–69.

    Article  CAS  PubMed  Google Scholar 

  71. Xu S, Zhang L, Cheng X, Yu H, Bao J, Lu R. Capsaicin inhibits the metastasis of human papillary thyroid carcinoma BCPAP cells through the modulation of the TRPV1 channel. Food Funct. 2018;9(1):344–54.

    Article  CAS  PubMed  Google Scholar 

  72. Kalluri R. The biology and function of fibroblasts in cancer. Nat Rev Cancer. 2016;16(9):582–98.

    Article  CAS  PubMed  Google Scholar 

  73. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006;6(5):392–401.

    Article  CAS  PubMed  Google Scholar 

  74. Atsumi T, Singh R, Sabharwal L, Bando H, Meng J, Arima Y, et al. Inflammation amplifier, a new paradigm in cancer biology. Can Res. 2014;74(1):8–14.

    Article  CAS  Google Scholar 

  75. Wang S, Liu Z, Wang L, Zhang X. NF-kappaB signaling pathway, inflammation and colorectal cancer. Cell Mol Immunol. 2009;6(5):327–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Munaron L. Intracellular calcium, endothelial cells and angiogenesis. Recent Pat Anti-Cancer Drug Discovery. 2006;1(1):105–19.

    Article  CAS  PubMed  Google Scholar 

  77. Earley S, Brayden JE. Transient receptor potential channels in the vasculature. Physiol Rev. 2015;95(2):645–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Faehling M, Kroll J, Föhr KJ, Fellbrich G, Mayr U, Trischler G, et al. Essential role of calcium in vascular endothelial growth factor A-induced signaling: mechanism of the antiangiogenic effect of carboxyamidotriazole. FASEB J. 2002;16(13):1805–7.

    Article  CAS  PubMed  Google Scholar 

  79. Moccia F, Negri S, Shekha M, Faris P, Guerra G. Endothelial Ca(2+) signaling, angiogenesis and vasculogenesis: just what it takes to make a blood vessel. Int J Mol Sci. 2019;20(16):3962.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Negri S, Faris P, Rosti V, Antognazza MR, Lodola F, Moccia F. Endothelial TRPV1 as an emerging molecular target to promote therapeutic angiogenesis. Cells. 2020;9(6):1341.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Voets T, Prenen J, Vriens J, Watanabe H, Janssens A, Wissenbach U, et al. Molecular determinants of permeation through the cation channel TRPV4. J Biol Chem. 2002;277(37):33704–10.

    Article  CAS  PubMed  Google Scholar 

  82. Watanabe H, Vriens J, Janssens A, Wondergem R, Droogmans G, Nilius B. Modulation of TRPV4 gating by intra- and extracellular Ca2+. Cell Calcium. 2003;33(5–6):489–95.

    Article  CAS  PubMed  Google Scholar 

  83. Zhao P, Lieu T, Barlow N, Metcalf M, Veldhuis NA, Jensen DD, et al. Cathepsin S causes inflammatory pain via biased agonism of PAR2 and TRPV4. J Biol Chem. 2014;289(39):27215–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Walter BA, Purmessur D, Moon A, Occhiogrosso J, Laudier DM, Hecht AC, et al. Reduced tissue osmolarity increases TRPV4 expression and pro-inflammatory cytokines in intervertebral disc cells. Eur Cell Mater. 2016;32:123–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S, Kim Y, et al. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature. 2009;457(7225):102–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Tang B, Wu J, Zhu MX, Sun X, Liu J, Xie R, et al. VPAC1 couples with TRPV4 channel to promote calcium-dependent gastric cancer progression via a novel autocrine mechanism. Oncogene. 2019;38(20):3946–61.

    Article  CAS  PubMed  Google Scholar 

  87. Cappelli HC, Kanugula AK, Adapala RK, Amin V, Sharma P, Midha P, et al. Mechanosensitive TRPV4 channels stabilize VE-cadherin junctions to regulate tumor vascular integrity and metastasis. Cancer Lett. 2019;442:15–20.

    Article  CAS  PubMed  Google Scholar 

  88. Shi M, Du F, Liu Y, Li L, Cai J, Zhang GF, et al. Glial cell-expressed mechanosensitive channel TRPV4 mediates infrasound-induced neuronal impairment. Acta Neuropathol. 2013;126(5):725–39.

    Article  CAS  PubMed  Google Scholar 

  89. Ye L, Kleiner S, Wu J, Sah R, Gupta RK, Banks AS, et al. TRPV4 is a regulator of adipose oxidative metabolism, inflammation, and energy homeostasis. Cell. 2012;151(1):96–110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Thodeti CK, Matthews B, Ravi A, Mammoto A, Ghosh K, Bracha AL, et al. TRPV4 channels mediate cyclic strain-induced endothelial cell reorientation through integrin-to-integrin signaling. Circ Res. 2009;104(9):1123–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Nan L, Zheng Y, Liao N, Li S, Wang Y, Chen Z, et al. Mechanical force promotes the proliferation and extracellular matrix synthesis of human gingival fibroblasts cultured on 3D PLGA scaffolds via TGF-β expression. Mol Med Rep. 2019;19(3):2107–14.

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Romani P, Valcarcel-Jimenez L, Frezza C, Dupont S. Crosstalk between mechanotransduction and metabolism. Nat Rev Mol Cell Biol. 2021;22(1):22–38.

    Article  CAS  PubMed  Google Scholar 

  93. Iskratsch T, Wolfenson H, Sheetz MP. Appreciating force and shape—the rise of mechanotransduction in cell biology. Nat Rev Mol Cell Biol. 2014;15(12):825–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Campellone KG, Welch MD. A nucleator arms race: cellular control of actin assembly. Nat Rev Mol Cell Biol. 2010;11(4):237–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Hotulainen P, Lappalainen P. Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J Cell Biol. 2006;173(3):383–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Riveline D, Zamir E, Balaban NQ, Schwarz US, Ishizaki T, Narumiya S, et al. Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J Cell Biol. 2001;153(6):1175–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Jiang G, Huang AH, Cai Y, Tanase M, Sheetz MP. Rigidity sensing at the leading edge through alphavbeta3 integrins and RPTPalpha. Biophys J. 2006;90(5):1804–9.

    Article  CAS  PubMed  Google Scholar 

  98. Roca-Cusachs P, Iskratsch T, Sheetz MP. Finding the weakest link: exploring integrin-mediated mechanical molecular pathways. J Cell Sci. 2012;125(Pt 13):3025–38.

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Rognoni L, Stigler J, Pelz B, Ylänne J, Rief M. Dynamic force sensing of filamin revealed in single-molecule experiments. Proc Natl Acad Sci USA. 2012;109(48):19679–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Prager-Khoutorsky M, Lichtenstein A, Krishnan R, Rajendran K, Mayo A, Kam Z, et al. Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing. Nat Cell Biol. 2011;13(12):1457–65.

    Article  CAS  PubMed  Google Scholar 

  101. Mohammadi H, Sahai E. Mechanisms and impact of altered tumour mechanics. Nat Cell Biol. 2018;20(7):766–74.

    Article  CAS  PubMed  Google Scholar 

  102. Hannigan G, Troussard AA, Dedhar S. Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat Rev Cancer. 2005;5(1):51–63.

    Article  CAS  PubMed  Google Scholar 

  103. Grootaert MOJ, Moulis M, Roth L, Martinet W, Vindis C, Bennett MR, et al. Vascular smooth muscle cell death, autophagy and senescence in atherosclerosis. Cardiovasc Res. 2018;114(4):622–34.

    Article  CAS  PubMed  Google Scholar 

  104. Mehta HM, Malandra M, Corey SJ. G-CSF and GM-CSF in neutropenia. J Immunol. 2015;195(4):1341–9.

    Article  CAS  PubMed  Google Scholar 

  105. Hasday JD, Garrison A, Singh IS, Standiford T, Ellis GS, Rao S, et al. Febrile-range hyperthermia augments pulmonary neutrophil recruitment and amplifies pulmonary oxygen toxicity. Am J Pathol. 2003;162(6):2005–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Capitano ML, Nemeth MJ, Mace TA, Salisbury-Ruf C, Segal BH, McCarthy PL, et al. Elevating body temperature enhances hematopoiesis and neutrophil recovery after total body irradiation in an IL-1-, IL-17-, and G-CSF-dependent manner. Blood. 2012;120(13):2600–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Ostberg JR, Repasky EA. Comparison of the effects of two different whole body hyperthermia protocols on the distribution of murine leukocyte populations. Int J Hyperther. 2000;16(1):29–43.

    Article  CAS  Google Scholar 

  108. Tulapurkar ME, Almutairy EA, Shah NG, He JR, Puche AC, Shapiro P, et al. Febrile-range hyperthermia modifies endothelial and neutrophilic functions to promote extravasation. Am J Respir Cell Mol Biol. 2012;46(6):807–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Huse M. Mechanical forces in the immune system. Nat Rev Immunol. 2017;17(11):679–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Jairaman A, Othy S, Dynes JL, Yeromin AV, Zavala A, Greenberg ML, et al. Piezo1 channels restrain regulatory T cells but are dispensable for effector CD4(+) T cell responses. Sci Adv. 2021. https://doi.org/10.1126/sciadv.abg5859.

    Article  PubMed  PubMed Central  Google Scholar 

  111. Horn LA, Chariou PL, Gameiro SR, Qin H, Iida M, Fousek K, et al. Remodeling the tumor microenvironment via blockade of LAIR-1 and TGF-β signaling enables PD-L1-mediated tumor eradication. J Clin Investig. 2022. https://doi.org/10.1172/JCI155148.

    Article  PubMed  PubMed Central  Google Scholar 

  112. Mennens SFB, Bolomini-Vittori M, Weiden J, Joosten B, Cambi A, van den Dries K. Substrate stiffness influences phenotype and function of human antigen-presenting dendritic cells. Sci Rep. 2017;7(1):17511.

    Article  PubMed  PubMed Central  Google Scholar 

  113. Choi Y, Kwon JE, Cho YK. Dendritic cell migration is tuned by mechanical stiffness of the confining space. Cells. 2021;10(12):3362.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Chakraborty M, Chu K, Shrestha A, Revelo XS, Zhang X, Gold MJ, et al. Mechanical stiffness controls dendritic cell metabolism and function. Cell Rep. 2021;34(2): 108609.

    Article  CAS  PubMed  Google Scholar 

  115. Huang Z, Sun Z, Zhang X, Niu K, Wang Y, Zheng J, et al. Loss of stretch-activated channels, PIEZOs, accelerates non-small cell lung cancer progression and cell migration. 2019. Biosci Rep. https://doi.org/10.1042/BSR20181679.

  116. Pappu P, Madduru D, Chandrasekharan M, Modhukur V, Nallapeta S, Suravajhala P. Next generation sequencing analysis of lung cancer datasets: a functional genomics perspective. Indian J Cancer. 2016;53(1):1–7.

    Article  CAS  PubMed  Google Scholar 

  117. Harsch M, Bendrat K, Hofmeier G, Branscheid D, Niendorf A. A new method for histological microdissection utilizing an ultrasonically oscillating needle: demonstrated by differential mRNA expression in human lung carcinoma tissue. Am J Pathol. 2001;158(6):1985–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Chen X, Wanggou S, Bodalia A, Zhu M, Dong W, Fan JJ, et al. A feedforward mechanism mediated by mechanosensitive ion channel PIEZO1 and tissue mechanics promotes glioma aggression. Neuron. 2018;100(4):799-815.e7.

    Article  CAS  PubMed  Google Scholar 

  119. Zhang J, Zhou Y, Huang T, Wu F, Liu L, Kwan JSH, et al. PIEZO1 functions as a potential oncogene by promoting cell proliferation and migration in gastric carcinogenesis. Mol Carcinog. 2018;57(9):1144–55.

    Article  CAS  PubMed  Google Scholar 

  120. Xu H, Chen Z, Li C. The prognostic value of Piezo1 in breast cancer patients with various clinicopathological features. Anticancer Drugs. 2021;32(4):448–55.

    Article  CAS  PubMed  Google Scholar 

  121. Lou W, Liu J, Ding B, Jin L, Xu L, Li X, et al. Five miRNAs-mediated PIEZO2 downregulation, accompanied with activation of Hedgehog signaling pathway, predicts poor prognosis of breast cancer. Aging. 2019;11(9):2628–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Han Y, Liu C, Zhang D, Men H, Huo L, Geng Q, et al. Mechanosensitive ion channel Piezo1 promotes prostate cancer development through the activation of the Akt/mTOR pathway and acceleration of cell cycle. Int J Oncol. 2019;55(3):629–44.

    CAS  PubMed  PubMed Central  Google Scholar 

  123. Etem E, Ceylan GG, Özaydın S, Ceylan C, Özercan I, Kuloğlu T. The increased expression of Piezo1 and Piezo2 ion channels in human and mouse bladder carcinoma. Adv Clin Experim Med. 2018;27(8):1025–31.

    Article  Google Scholar 

  124. De Felice D, Alaimo A. Mechanosensitive piezo channels in cancer: focus on altered calcium signaling in cancer cells and in tumor progression. Cancers. 2020;12(7):1780.

    Article  PubMed  PubMed Central  Google Scholar 

  125. Yang XN, Lu YP, Liu JJ, Huang JK, Liu YP, Xiao CX, et al. Piezo1 is as a novel trefoil factor family 1 binding protein that promotes gastric cancer cell mobility in vitro. Dig Dis Sci. 2014;59(7):1428–35.

    Article  CAS  PubMed  Google Scholar 

  126. Li C, Rezania S, Kammerer S, Sokolowski A, Devaney T, Gorischek A, et al. Piezo1 forms mechanosensitive ion channels in the human MCF-7 breast cancer cell line. Sci Rep. 2015;5:8364.

    Article  PubMed  PubMed Central  Google Scholar 

  127. Liu CSC, Ganguly D. Mechanical cues for T Cell Activation: role of Piezo1 mechanosensors. Crit Rev Immunol. 2019;39(1):15–38.

    Article  PubMed  Google Scholar 

  128. Forget A, Gianni-Barrera R, Uccelli A, Sarem M, Kohler E, Fogli B, et al. Mechanically defined microenvironment promotes stabilization of microvasculature, which correlates with the enrichment of a novel Piezo-1(+) population of circulating CD11b(+) /CD115(+) monocytes. Adv Mater. 2019;31(21): e1808050.

    Article  PubMed  Google Scholar 

  129. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science (New York, NY). 1997;275(5302):964–7.

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by grants from the National Nature Science Foundation of China (82072985), Heilongjiang Province Innovation Base Award Project (JD2023SJ03), Wu-Jieping Medical Foundation (320.6750.19089-22,320.6750.19089-48), Beijing Medical Award Foundation (YXJL-2019-1416-0069), Hai Yan Youth Fund of Harbin Medical University Cancer Hospital (JJQN2021-02), the Fundamental Research Funds for the Provincial Universities (2021-KYYWF-0253), Natural Science Foundation of Heilongjiang Province (LH2022H065), Scientific research project of the Heilongjiang Provincial Health Commission (20210808020126).

Author information

Authors and Affiliations

Authors

Contributions

Yun-jing Hou, Xin-xin Yang, Lin He, and Hong-xue Meng. Yun-jing Hou, Xin-xin Yang reviewed the literature and wrote the first draft. Lin He contributed to the conception and design of the manuscript. Hong-xue Meng administrated and finalized the manuscript. All authors read and approved the final version of the manuscript. Data authentication is not applicable.

Corresponding author

Correspondence to Hong-xue Meng.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hou, Yj., Yang, Xx., He, L. et al. Pathological mechanisms of cold and mechanical stress in modulating cancer progression. Human Cell 37, 593–606 (2024). https://doi.org/10.1007/s13577-024-01049-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13577-024-01049-y

Keywords

Navigation