Laminin chains in rat and human peripheral nerve: Distribution and regulation during development and after axonal injury

Journal of Comparative Neurology

Volumn 454, Issue 3, 2002, Pages 284-293

  Wallquist, Wilhelm ^a   Patarroyo, Manuel ^a   Thams, Sebastian ^a   Carlstedt, Thomas ^a,b   Stark, Birgit ^a   Cullheim, Staffan ^a   Hammarberg, Henrik ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b ROYAL NATIONAL ORTHOPAEDIC HOSPITAL   (United Kingdom)

Author keywords

Extracellular matrix; Immunohistochemistry; In situ hybridization; Nerve regeneration; Schwann cells

Indexed keywords

INTEGRIN; ISOPROTEIN; LAMININ; MESSENGER RNA; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; CASE REPORT; CONTROLLED STUDY; HISTOCHEMISTRY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NERVE CRUSH; NERVE FIBER REGENERATION; NERVE GROWTH; NERVE TRANSECTION; NERVOUS SYSTEM DEVELOPMENT; NEUROFILAMENT; NEWBORN; NONHUMAN; PERINEURIUM; PERIPHERAL NERVE INJURY; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SPINAL CORD MOTONEURON; UPREGULATION;

ANIMALS; ANIMALS, NEWBORN; AXONS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; LAMININ; PERIPHERAL NERVES; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NEUROPATHY;

EID: 0037121764     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10434     Document Type: Article

References (87)

1. Acheson A, Edgar D, Timpl R, Thoenen H. 1986. Laminin increases both levels and activity of tyrosine hydroxylase in calf adrenal chromaffin cells. J Cell Biol 102:151-159.
2. Adler R, Jerdan J, Hewitt AT. 1985. Responses of cultured neural retinal cells to substratum-bound laminin and other extracellular matrix molecules. Dev Biol 112:100-114.
3. Agius E, Sagot Y, Duprat AM, Cochard P. 1996. Antibodies directed against the beta 1-integrin subunit and peptides containing the IKVAV sequence of laminin perturb neurite outgrowth of peripheral neurons on immature spinal cord substrata. Neuroscience 71:773-786.
4. Anton ES, Sandrock AW Jr, Matthew WD. 1994. Merosin promotes neurite growth and Schwann cell migration in vitro and nerve regeneration in vivo: Evidence using an antibody to merosin, ARM-1. Dev Biol 164:133-146.
5. Anton ES, Kreidberg JA, Rakic P. 1999. Distinct functions of alpha3 and alpha(v) integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron 22:277-289.
6. Ashcroft GS. 1999. Bidirectional regulation of macrophage function by TGF-beta. Microbes Infect 1:1275-1282.
7. Baker SE, Hopkinson SB, Fitchmun M, Andreason GL, Frasier F, Plopper G, Quaranta V, Jones JC. 1996. Laminin-5 and hemidesmosomes: Role of the alpha 3 chain subunit in hemidesmosome stability and assembly. J Cell Sci 109:2509-2520.
8. Bates CA, Meyer RL. 1997. The neurite-promoting effect of laminin is mediated by different mechanisms in embryonic and adult regenerating mouse optic axons in vitro. Dev Biol 181:91-101.
9. Bernier SM, Utani A, Sugiyama S, Doi T, Polistina C, Yamada Y. 1995. Cloning and expression of laminin alpha 2 chain (M-chain) in the mouse. Matrix Biol 14:447-455.
10. Bonaldo MF, Lennon G, Soares MB. 1996. Normalization and subtraction: Two approaches to facilitate gene discovery. Genome Res 6:791-806.
11. Bronner-Fraser M, Artinger M, Muschler J, Horwitz AF. 1992. Developmentally regulated expression of alpha 6 integrin in avian embryos. Development 115:197-211.
12. Bruck W. 1997. The role of macrophages in Wallerian degeneration. Brain Pathol 7:741-752.
13. Bunge RP. 1993. Expanding roles for the Schwann cell: Ensheathment, myelination, trophism and regeneration. Curr Opin Neurobiol 3:805-809.
14. Calof AL, Campanero MR, O'Rear JJ, Yurchenco PD, Lander AD. 1994. Domain-specific activation of neuronal migration and neurite outgrowth- promoting activities of laminin. Neuron 13:117-130.
15. Cho SI, Ko J, Patton BL, Sanes JR, Chiu AY. 1998. Motor neurons and Schwann cells distinguish between synaptic and extrasynaptic isoforms of laminin. J Neurobiol 37:339-358.
16. Colognato H, Yurchenco PD. 2000. Form and function: The laminin family of heterotrimers. Dev Dyn 218:213-234.
17. Colognato H, MacCarrick M, O'Rear JJ, Yurchenco PD. 1997. The laminin alpha2-chain short arm mediates cell adhesion through both the alpha1beta1 and alpha2beta1 integrins. J Biol Chem 272:29330-29336.
18. Cornbrooks CJ, Carey DJ, McDonald JA, Timpl R, Bunge RP. 1983. In vivo and in vitro observations on laminin production by Schwann cells. Proc Natl Acad Sci U S A 80:3850-3854.
19. Dagerlind A, Friberg K, Bean AJ, Hökfelt T. 1992. Sensitive mRNA detection using unfixed tissue: Combined radioactive and non-radioactive in situ hybridization histochemistry. Histochemistry 98:39-49.
20. de Curtis I. 1993. The alpha 6 beta 1 integrin is a laminin receptor for developing retinal neurons. Cytotechnology 11:S41-S43.
21. Doyu M, Sobue G, Ken E, Kimata K, Shinomura T, Yamada Y, Mitsuma T, Takahashi A. 1993. Laminin A, B1, and B2 chain gene expression in transected and regenerating nerves: Regulation by axonal signals. J Neurochem 60:543-551.
22. Edgar D, Carter J, Runswick S, Ybot P. 1994. Role of laminin for axonal growth. Eur Arch Otorhinolaryngol Suppl:S60-S61.
23. Einheber S, Milner TA, Giancotti F, Salzer JL. 1993. Axonal regulation of Schwann cell integrin expression suggests a role for alpha 6 beta 4 in myelination. J Cell Biol 123:1223-1236.
24. Engvall E, Davis GE, Dickerson K, Ruoslahti E, Varon S, Manthorpe M. 1986. Mapping of domains in human laminin using monoclonal antibodies: Localization of the neurite-promoting site. J Cell Biol 103:2457-2465.
25. Engvall E, Earwicker D, Day A, Muir D, Manthorpe M, Paulsson M. 1992. Merosin promotes cell attachment and neurite outgrowth and is a component of the neurite-promoting factor of RN22 schwannoma cells. Exp Cell Res 198:115-123.
26. Faivre-Bauman A, Puymirat J, Loudes C, Barret A, Tixier-Vidal A. 1984. Laminin promotes attachment and neurite elongation of fetal hypothalamic neurons grown in serum-free medium. Neurosci Lett 44:83-89.
27. Fernandez-Valle C, Fregien N, Wood PM, Bunge MB. 1993. Expression of the protein zero myelin gene in axon-related Schwann cells is linked to basal lamina formation. Development 119:867-880.
28. Fernandez-Valle C, Gwynn L, Wood PM, Carbonetto S, Bunge MB. 1994. Anti-beta 1 integrin antibody inhibits Schwann cell myelination. J Neurobiol 25:1207-1226.
29. Geberhiwot T, Ingerpuu S, Pedraza C, Neira M, Lehto U, Virtanen I, Kortesmaa J, Tryggvason K, Engvall E, Patarroyo M. 1999. Blood platelets contain and secrete laminin-8 (alpha4beta1gamma1) and adhere to laminin-8 via alpha6beta1 integrin. Exp Cell Res 253:723-732.
30. Gessani S, Belardelli F. 1998. IFN-gamma expression in macrophages and its possible biological significance. Cytokine Growth Factor Rev 9:117-123.
31. Gibson JD. 1979. The origin of the neural macrophage: A quantitative ultrastructural study of cell population changes during Wallerian degeneration. J Anat 129:1-19.
32. Hammarberg H, Risling M, Hokfelt T, Cullheim S, Piehl F. 1998. Expression of insulin-like growth factors and corresponding binding proteins (IGFBP 1-6) in rat spinal cord and peripheral nerve after axonal injuries. J Comp Neurol 400:57-72.
33. Hammarberg H, Piehl F, Risling M, Cullheim S. 2000a. Differential regulation of trophic factor receptor mRNAs in spinal motoneurons after sciatic nerve transection and ventral root avulsion in the rat. J Comp Neurol 426:587-601.
34. Hammarberg H, Wallquist W, Piehl F, Risling M, Cullheim S. 2000b. Regulation of laminin-associated integrin subunit mRNAs in rat spinal motoneurons during postnatal development and after axonal injury. J Comp Neurol 428:294-304.
35. Hsiao LL, Engvall E, Peltonen J, Uitto J. 1993. Expression of laminin isoforms by peripheral nerve-derived connective tissue cells in culture. Comparison with epitope distribution in normal human nerve and neural tumors in vivo. Lab Invest 68:100-108.
36. Hunter DD, Shah V, Merlie JP, Sanes JR. 1989. A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction. Nature 338:229-234.
37. Iivanainen A, Morita T, Tryggvason K. 1999. Molecular cloning and tissue-specific expression of a novel murine laminin gamma3 chain. J Biol Chem 274:14107-14111.
38. Kalcheim C, Barde YA, Thoenen H, Le Douarin NM. 1987. In vivo effect of brain-derived neurotrophic factor on the survival of developing dorsal root ganglion cells. EMBO J 6:2871-2873.
39. Koch M, Olson PF, Albus A, Jin W, Hunter DD, Brunken WJ, Burgeson RE, Champliaud MF. 1999. Characterization and expression of the laminin gamma3 chain: A novel, non-basement membrane-associated, laminin chain. J Cell Biol 145:605-618.
40. Kortesmaa J, Yurchenco P, Tryggvason K. 2000. Recombinant Laminin-8 (alpha 4beta 1gamma 1). Production, purification, and interactions with integrins. J Biol Chem 275:14853-14859.
41. Kuang W, Xu H, Vachon PH, Liu L, Loechel F, Wewer UM, Engvall E. 1998. Merosin-deficient congenital muscular dystrophy. Partial genetic correction in two mouse models. J Clin Invest 102:844-852.
42. Kuecherer-Ehret A, Graeber MB, Edgar D, Thoenen H, Kreutzberg GW. 1990. Immunoelectron microscopic localization of laminin in normal and regenerating mouse sciatic nerve. J Neurocytol 19:101-109.
43. Leivo I, Engvall E. 1988. Merosin, a protein specific for basement membranes of Schwann cells, striated muscle, and trophoblast, is expressed late in nerve and muscle development. Proc Natl Acad Sci U S A 85:1544-1548.
44. Lentz SI, Miner JH, Sanes JR, Snider WD. 1997. Distribution of the 10 known laminin chains in the pathways and targets of developing sensory axons. J Comp Neurol 378:547-561.
45. Libby RT, Champliaud MF, Claudepierre T, Xu Y, Gibbons EP, Koch M, Burgeson RE, Hunter DD, Brunken WJ. 2000. Laminin expression in adult and developing retinae: Evidence of two novel CNS laminins. J Neurosci 20:6517-6528.
46. Liesi P, Risteli L. 1989. Glial cells of mammalian brain produce a variant form of laminin. Exp Neurol 105:86-92.
47. Liesi P, Dahl D, Vaheri A. 1984. Neurons cultured from developing rat brain attach and spread preferentially to laminin. J Neurosci Res 11:241-251.
48. Liu HM, Yang LH, Yang YJ. 1995. Schwann cell properties: 3. C-fos expression, bFGF production, phagocytosis and proliferation during Wallerian degeneration. J Neuropathol Exp Neurol 54:487-496.
49. Manthorpe M, Engvall E, Ruoslahti E, Longo FM, Davis GE, Varon S. 1983. Laminin promotes neuritic regeneration from cultured peripheral and central neurons. J Cell Biol 97:1882-1890.
50. McGarvey ML, Baron-Van Evercooren A, Kleinman HK, Dubois-Dalcq M. 1984. Synthesis and effects of basement membrane components in cultured rat Schwann cells. Dev Biol 105:18-28.
51. Milner R, Wilby M, Nishimura S, Boylen K, Edwards G, Fawcett J, Streuli C, Pytela R, ffrench-Constant C. 1997. Division of labor of Schwann cell integrins during migration on peripheral nerve extracellular matrix ligands. Dev Biol 185:215-228.
52. Miner JH, Patton BL, Lentz SI, Gilbert DJ, Snider WD, Jenkins NA, Copeland NG, Sanes JR. 1997. The laminin alpha chains: Expression, developmental transitions, and chromosomal locations of alpha1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel alpha3 isoform. J Cell Biol 137:685-701.
53. Nacy CA, Meierovics AI, Belosevic M, Green SJ. 1991. Tumor necrosis factor-alpha: Central regulatory cytokine in the induction of macrophage antimicrobial activities. Pathobiology 59:182-184.
54. Nakagawa M, Miyagoe-Suzuki Y, Ikezoe K, Miyata Y, Nonaka I, Harii K, Takeda S. 2001. Schwann cell myelination occurred without basal lamina formation in laminin alpha2 chain-null mutant (dy(3K)/dy(3K)) mice. Glia 35:101-110.
55. Obremski VJ, Bunge MB. 1995. Addition of purified basal lamina molecules enables Schwann cell ensheathment of sympathetic neurites in culture. Dev Biol 168:124-137.
56. Patton BL, Miner JH, Chiu AY, Sanes JR. 1997. Distribution and function of laminins in the neuromuscular system of developing, adult, and mutant mice. J Cell Biol 139:1507-1521.
57. Patton BL, Cunningham JM, Thyboll J, Kortesmaa J, Westerblad H, Edstrom L, Tryggvason K, Sanes JR. 2001. Properly formed but improperly localized synaptic specializations in the absence of laminin alpha4. Nat Neurosci 4:597-604.
58. Pedraza C, Geberhiwot T, Ingerpuu S, Assefa D, Wondimu Z, Kortesmaa J, Tryggvason K, Virtanen I, Patarroyo M. 2000. Monocytic cells synthe-size, adhere to, and migrate on laminin-8 (alpha 4 beta 1 gamma 1). J Immunol 165:5831-5838.
59. Petäjäniemi N, Korhonen M, Kortesmaa J, Tryggvason K, Sekiguchi K, Fujiwara H, Sorokin L, Thornell LE, Wondimu Z, Assefa D, Patarroyo M, Virtanen I. 2002. Localization of laminin α4-chain in developing and adult human tissues. J Histochem Cytochem 50:1113-1130.
60. Podratz JL, Rodriguez E, Windebank AJ. 2001. Role of the extracellular matrix in myelination of peripheral nerve. Glia 35:35-40.
61. Podratz JL, Rodriguez EH, DiNonno ES, Windebank AJ. 1998. Myelination by Schwann cells in the absence of extracellular matrix assembly. Glia 23:383-388.
62. Rajagopal S, Moskal TL, Wang H, Chakrabarty S. 1999. Efficacy and specificity of antisense laminin chain-specific expression vectors in blocking laminin induction by TGFbetal: Effect of laminin blockade on TGFbeta1-mediated cellular responses. J Cell Physiol 178:296-303.
63. Reichardt LF, Tomaselli KJ. 1991. Extracellular matrix molecules and their receptors: Functions in neural development. Annu Rev Neurosci 14:531-570.
64. Relvas JB, Setzu A, Baron W, Buttery PC, LaFlamme SE, Franklin RJ, ffrench-Constant C. 2001. Expression of dominant-negative and chimeric subunits reveals an essential role for betal integrin during myelination. Curr Biol 11:1039-1043.
65. Rogers SL, Letourneau PC, Palm SL, McCarthy J, Furcht LT. 1983. Neurite extension by peripheral and central nervous system neurons in response to substratum-bound fibronectin and laminin. Dev Biol 98: 212-220.
66. Salonen V, Peltonen J, Roytta M, Virtanen I. 1987. Laminin in traumatized peripheral nerve: Basement membrane changes during degeneration and regeneration. J Neurocytol 16:713-720.
67. Sanes JR, Engvall E, Butkowski R, Hunter DD. 1990. Molecular heterogeneity of basal laminae: Isoforms of laminin and collagen IV at the neuromuscular junction and elsewhere. J Cell Biol 111:1685-1699.
68. Sasaki M, Kato S, Kohno K, Martin GR, Yamada Y. 1987. Sequence of the cDNA encoding the laminin B1 chain reveals a multidomain protein containing cysteine-rich repeats. Proc Natl Acad Sci U S A 84:935-939.
69. Sasaki M, Kleinman HK, Huber H, Deutzmann R, Yamada Y. 1988. Laminin, a multidomain protein. The A chain has a unique globular domain and homology with the basement membrane proteoglycan and the laminin B chains. J Biol Chem 263:16536-16544.
70. Schober S, Mielenz D, Echtermeyer F, Hapke S, Poschl E, von der Mark H, Moch H, von der Mark K. 2000. The role of extracellular and cytoplasmic splice domains of alpha7-integrin in cell adhesion and migration on laminins. Exp Cell Res 255:303-313.
71. Seebacher T, Medina JL, Bade EG. 1997. Laminin alpha 5, a major transcript of normal and malignant rat liver epithelial cells, is differentially expressed in developing and adult liver. Exp Cell Res 237:70-76.
72. Siironen J, Sandberg M, Vuorinen V, Roytta M. 1992. Laminin B1 and collagen type IV gene expression in transected peripheral nerve: Reinnervation compared to denervation. J Neurochem 59:2184-2192.
73. Stoll G, Muller HW. 1999. Nerve injury, axonal degeneration and neural regeneration: Basic insights. Brain Pathol 9:313-325.
74. Stoll G, Griffin JW, Li CY, Trapp BD. 1989. Wallerian degeneration in the peripheral nervous system: Participation of both Schwann cells and macrophages in myelin degradation. J Neurocytol 18:671-683.
75. Sugiyama S, Utani A, Yamada S, Kozak CA, Yamada Y. 1995. Cloning and expression of the mouse laminin gamma 2 (B2t) chain, a subunit of epithelial cell laminin. Eur J Biochem 228:120-128.
76. Talts JF, Sasaki T, Miosge N, Gohring W, Mann K, Mayne R, Timpl R. 2000. Structural and functional analysis of the recombinant G domain of the laminin alpha4 chain and its proteolytic processing in tissues. J Biol Chem 275:35192-35199.
77. Tiger CF, Champliaud MF, Pedrosa-Domellof F, Thornell LE, Ekblom P, Gullberg D. 1997. Presence of laminin alpha5 chain and lack of laminin alphal chain during human muscle development and in muscular dystrophies. J Biol Chem 272:28590-28595.
78. Tome FM, Evangelista T, Leclerc A, Sunada Y, Manole E, Estournet B, Barois A, Campbell KP, Fardeau M. 1994. Congenital muscular dystrophy with merosin deficiency. C R Acad Sci III 317:351-357.
79. Unsicker K, Skaper SD, Davis GE, Manthorpe M, Varon S. 1985. Comparison of the effects of laminin and the polyornithine-binding neurite promoting factor from RN22 Schwannoma cells on neurite regeneration from cultured newborn and adult rat dorsal root ganglion neurons. Brain Res 349:304-308.
80. Utani A, Kopp JB, Kozak CA, Matsuki Y, Amizuka N, Sugiyama S, Yamada Y. 1995. Mouse kalinin B1 (laminin beta 3 chain): Cloning and tissue distribution. Lab Invest 72:300-310.
81. Uziyel Y, Hall S, Cohen J. 2000. Influence of laminin-2 on Schwann cell-axon interactions. Glia 32:109-121. Van den Heuvel GB, Leardkamolkarn V, St John PL, Abrahamson DR. 1996. Carboxy terminal sequence and synthesis of rat kidney laminin gamma 1 chain. Kidney Int 49:752-760.
82. Virtanen I, Gullberg D, Rissanen J, Kivilaakso E, Kiviluoto T, Laitinen LA, Lehto VP, Ekblom P. 2000. Laminin alpha1-chain shows a restricted distribution in epithelial basement membranes of fetal and adult human tissues. Exp Cell Res 257:298-309.
83. Virtanen I, Lohi J, Tani T, Korhonen M, Burgeson RE, Lehto VP, Leivo I. 1997. Distinct changes in the laminin composition of basement membranes in human seminiferous tubules during development and degeneration. Am J Pathol 150:1421-1431.
84. Weaver CD, Yoshida CK, de Curtis I, Reichardt LF. 1995. Expression and in vitro function of beta 1-integrin laminin receptors in the developing avian ciliary ganglion [published erratum appears in J Neurosci 1996;16:7097-7098]. J Neurosci 15:5275-5285.
85. Yamada H, Chiba A, Endo T, Kobata A, Anderson LV, Hori H, Fukuta-Ohi H, Kanazawa I, Campbell KP, Shimizu T, Matsumura K. 1996. Characterization of dystroglycan-laminin interaction in peripheral nerve. J Neurochem 66:1518-1524.
86. Yang CW, Hattori M, Vlassara H, He CJ, Carome MA, Yamato E, Elliot S, Striker GE, Striker LJ. 1995. Overexpression of transforming growth factor-beta 1 mRNA is associated with up-regulation of glomerular tenascin and laminin gene expression in nonobese diabetic mice. J Am Soc Nephrol 5:1610-1617.
87. Zhang XH, Sun HM, Yuan JQ. 2001. Extracellular matrix production of lens epithelial cells. J Cataract Refract Surg 27:1303-1309.