Trends in Cell Biology
Volume 13, Issue 4, April 2003, Pages 187-194
Journal home page for Trends in Cell Biology

Nogo and its paRTNers

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Abstract

Reticulons (RTNs) are a relatively new eukaryotic gene family with unknown functions but broad expression and peculiar topological features. RTNs are widely distributed in plants, yeast and animals and are characterized by a ∼200-amino-acid C-terminal domain, including two long hydrophobic sequences. Nogo/RTN4 can inhibit neurite growth from the cell surface via specific receptors, whereas more general, ‘ancestral’, RTN functions might relate to those of the endoplasmic reticulum – for example, intracellular trafficking, cell division and apoptosis. Here, we review the taxonomic distribution and tissue expression of RTNs, summarize recent discoveries about RTN localization and membrane topology, and discuss the possible functions of RTNs.

Section snippets

Taxonomic distribution and evolution of the RTN family

Genes for RTN-like proteins have been identified in most eukaryotic taxa and have evolved from an intron-rich ancestor (T. Oertle, unpublished). In prokaryotes, no homologues have been identified so far, suggesting that RTNs emerged relatively recently in eukaryotes, potentially in parallel with the evolution of the endomembrane system (T. Oertle, unpublished). There are four mammalian reticulon genes (RTN1, RTN2, RTN3 and Nogo/RTN4), each of which can give rise to a range of alternative

Tissue expression of mammalian RTN genes

The four mammalian RTN genes have a broad tissue expression pattern (Table 1) Most transcripts are enriched in nervous tissues (RTN1-A, RTN1-C, RTN2-A, RTN2-B, Nogo-A/RTN4-A). The RTN1 transcripts are almost exclusively expressed in neurons and neuroendocrine cells. Nogo-A/RTN4-A is expressed by oligodendrocytes, the myelin-forming cells of the adult CNS, and some neuronal subpopulations, heart and testis (Table 1). Two RTN transcripts (RTN2-C, Nogo-C/RTN4-C) are particularly enriched in

Subcellular localization

The shared feature of RTN proteins is their association with membranes of the endoplasmic reticulum (ER) [3] (Fig. 2b). This has been shown for mammalian RTN1 3, 15, RTN3 [16] and Nogo/RTN4 (4, 6; T. Oertle, unpublished) as well as for Drosophila Rtnl1 [17] and Caenorhabditis RTNL [18]. Because all RTNs lack a canonical leader peptide at their N-termini, translocation into the ER is assumed to be directed by internal signals (e.g. transmembrane domains). Alternatively, the ER association could

Membrane topology

The membrane topology of RTNs is of specific interest, particularly because the two very large (∼35 amino acid) putative transmembrane domains could both span the membrane either once or twice (Fig. 2). Immunofluorescence studies have shown that, in the prevalent ER-associated topology, the N- and C-termini of RTNs face the cytoplasm (6, 16; M. van der Haar, unpublished) (Fig. 2a). The 66-amino-acid loop between the two hydrophobic domains of Nogo-A cannot be detected by antibodies without

RTNs as marker proteins and their roles in neuronal differentiation

RTN1-A and RTN1-C are both expressed in most neuroendocrine tumours, such as SCLCs, whereas they are absent in atypical carcinoids 25, 26, 27. Only non-SCLCs showing a neuroendocrine immunophenotype also produce RTN1-A [28]. Thus, RTN1 is considered to be a highly sensitive and specific marker of neuroendocrine differentiation in lung cancer to be used in the diagnosis of this disease. Although it has been speculated that the presence of neuroendocrine markers could help to identify patients

ER function, plasma-membrane formation and cell division

Because RTNs are found in almost all eukaryotic cells and organisms, they would be expected to exert basic functions in the cellular machinery. Single RTN genes seem not to be of vital importance, however, because organisms with RTN gene disruptions (Saccharomyces cerevisiae, Schizosaccharomyces pombe, Caenorhabditis elegans and Drosophila melanogaster) are viable (e.g. 17, 18, 40). On the basis of the (few) existing data, the following hypotheses for cellular functions of RTN proteins can be

Concluding remarks

Research in the field of RTNs has increasingly moved beyond descriptive studies of their expression patterns and genomic structures towards functional enquiries. The role of Nogo in neurite-outgrowth inhibition is currently being studied extensively. By contrast, the roles of RTN1, RTN2 and RTN3 in vertebrates, the possible intracellular role of Nogo/RTN4, and the function of the RTN genes in invertebrates, plants and yeast are poorly understood, and represent an exciting subject for future

Acknowledgements

We thank O. Gilliéron and D. Merkler for providing unpublished data to complete Table 1, M. van der Haar for providing Fig. 2c, and A. Buss, D. Merkler, M. Kerschensteiner and S. DeMarco for critically reading the manuscript. We also thank E. Hochreutener and R. Schöb for excellent graphical work. Our own studies were supported by the Swiss National Science Foundation (grant 31-63633) and by the NCCR on Neural Plasticity and Repair.

References (73)

  • D.F. Wieczorek et al.

    Developmentally regulated cDNA expressed exclusively in neural tissue

    Brain Res. Mol. Brain Res.

    (1991)
  • A.J. Roebroek

    Cloning and expression of alternative transcripts of a novel neuroendocrine-specific gene and identification of its 135-kDa translational product

    J. Biol. Chem.

    (1993)
  • H.J.K. van de Velde

    NSP-encoded reticulons, neuroendocrine proteins of a novel gene family associated with membranes of the endoplasmic reticulum

    J. Cell Sci.

    (1994)
  • M.S. Chen

    Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen form monoclonal antibody IN-1

    Nature

    (2000)
  • R. Prinjha

    Inhibitor of neurite outgrowth in humans

    Nature

    (2000)
  • T. Grand-Pré

    Identification of the Nogo inhibitor of axon regeneration as a reticulon protein

    Nature

    (2000)
  • Q. Li

    Link of a new type of apoptosis-inducing gene ASY/Nogo-B to human cancer

    Oncogene

    (2001)
  • A.B. Huber et al.

    Nogo-A, a potent inhibitor of neurite outgrowth and regeneration

    Biol. Chem.

    (2000)
  • P.A. Brittis et al.

    Nogo domains and a Nogo receptor: implications for axon regeneration

    Neuron

    (2001)
  • C.E. Ng et al.

    Nogos and the Nogo-66 receptor: factors inhibiting CNS neuron regeneration

    J. Neurosci. Res.

    (2002)
  • T. Oertle

    Genomic structure and functional characterisation of the promoters of human and mouse Nogo/Rtn-4

    J. Mol. Biol.

    (2003)
  • J.G. Geisler

    Molecular cloning of a novel mouse gene with predominant muscle and neural expression

    Mamm. Genome

    (1998)
  • A.J. Roebroek

    Genomic organization of the human NSP gene, prototype of a novel gene family encoding reticulons

    Genomics

    (1996)
  • S. Panda

    Coordinated transcription of key pathways in the mouse by the circadian clock

    Cell

    (2002)
  • N.H. Senden

    Subcellular localization and supramolecular organization of neuroendocrine-specific protein B (NSP-B) in small cell lung cancer

    Eur. J. Cell Biol.

    (1994)
  • N. Hamada

    Molecular cloning and characterization of the mouse reticulon 3 cDNA

    Cell. Mol. Biol.

    (2002)
  • X. Morin

    A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila

    Proc. Natl. Acad. Sci. U. S. A.

    (2001)
  • J. Iwahashi

    Caenorhabditis elegans reticulon interacts with RME-1 during embryogenesis

    Biochem. Biophys. Res. Commun.

    (2002)
  • Oertle, T. et al. Do cancer cells die because of Nogo-B? Oncogene (in...
  • J.G. Geisler

    Nspl1, a new Z-band-associated protein

    J. Muscle Res. Cell Motil.

    (1999)
  • I.D. Baka

    Intracellular compartmentalization of two differentially spliced s-rex/NSP mRNAs in neurons

    Mol. Cell. Neurosci.

    (1996)
  • N.N. Ninkina

    Rat and chicken s-rex/NSP mRNA: nucleotide sequence of main transcripts and expression of splice variants in rat tissues

    Gene

    (1997)
  • N.H. Senden

    Neuroendocrine-specific protein C (NSP-C): subcellular localization and differential expression in relation to NSP-A

    Eur. J. Cell Biol.

    (1996)
  • H. Tozaki

    Expression of Nogo protein by growing axons in the developing nervous system

    Brain Res. Mol. Brain Res.

    (2002)
  • N.H. Senden

    Cluster-10 lung-cancer antibodies recognize NSPs, novel neuro-endocrine proteins associated with membranes of the endoplasmic reticulum

    Int. J. Cancer

    (1994)
  • H.J.K. van de Velde

    NSP-encoded reticulons are neuroendocrine markers of a novel category in human lung cancer diagnosis

    Cancer Res.

    (1994)
  • N.H. Senden

    A comparison of NSP-reticulons with conventional neuroendocrine markers in immunophenotyping of lung cancers

    J. Pathol.

    (1997)
  • N. Senden

    Neuroendocrine-specific protein (NSP)-reticulons as independent markers for non-small cell lung cancer with neuroendocrine differentiation. An in vitro histochemical study

    Histochem. Cell Biol.

    (1997)
  • A. Gajra

    The predictive value of neuroendocrine markers and p53 for response to chemotherapy and survival in patients with advanced non-small cell lung cancer

    Lung Cancer

    (2002)
  • J. Hens

    Neuronal differentiation is accompanied by NSP-C expression

    Cell Tissue Res.

    (1998)
  • Q. Li

    Identification of transcripts expressed under functional differentiation in primary culture of cerebral cortical neurons

    Neurochem. Res.

    (2002)
  • S.H. Kim

    Neuroendocrine-specific protein C, a marker of neuronal differentiation, is reduced in brain of patients with Down syndrome and Alzheimer's disease

    Biochem. Biophys. Res. Commun.

    (2000)
  • A.B. Huber

    Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions

    J. Neurosci.

    (2002)
  • A. Josephson

    Nogo mRNA expression in adult and fetal human and rat nervous tissue and in weight drop injury

    Exp. Neurol.

    (2001)
  • C. Magnusson

    Differential expression of Nogo (Reticulon 4) transcripts in innervated and denervated mouse skeletal muscle

    Soc. Neurosci. Abstr.

    (2001)
  • L. Dupuis

    Nogo provides a molecular marker for diagnosis of amyotrophic lateral sclerosis

    Neurobiol. Dis.

    (2002)
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