A human-mouse chimera of the α3α4α5(IV) collagen protomer rescues the renal phenotype in Col4a3-/- alport mice

American Journal of Pathology

Volumn 163, Issue 4, 2003, Pages 1633-1644

  Heidet, Laurence ^a,b   Borza, Dorin Bogdan ^c   Jouin, Mélanie ^a   Sich, Mireille ^a   Mattei, Marie Geneviève ^a   Sado, Yoshikazu ^d   Hudson, Billy G ^c   Hastie, Nicholas ^e   Antignac, Corinne ^a,b   Gubler, Marie Claire ^a  

^a INSERM   (France)

^b HÔPITAL NECKER ENFANTS MALADES   (France)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d Shigei Medical Research Institute   (Japan)

^e WESTERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4;

ALPORT SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CHIMERA; COL4A3 GENE; COL4A4 GENE; COL4A5 GENE; CONTROLLED STUDY; GENE; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GLOMERULUS BASEMENT MEMBRANE; GLOMERULUS FILTRATION; GOODPASTURE SYNDROME; HUMAN; HUMAN CELL; KIDNEY DISEASE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; TRANSGENIC MOUSE; YEAST ARTIFICIAL CHROMOSOME;

EID: 0141648351     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)63520-1     Document Type: Article

References (47)

1. Boutaud A, Borza DB, Bondar O, Gunwar S, Netzer KO, Singh N, Ninomiya Y, Sado Y, Noelken ME, Hudson BG: Type IV collagen of the glomerular basement membrane. Evidence that the chain specificity of network assembly is encoded by the noncollagenous NC1 domains. J Biol Chem 2000, 275:30716-30724
2. Borza DB, Bondar O, Todd P, Sundaramoorthy M, Sado Y, Ninomiya Y, Hudson BG: Quaternary organization of the Goodpasture autoantigen, the alpha 3(IV) collagen chain: sequestration of two cryptic autoepitopes by intra-protomer interactions with the alpha 4 and alpha 5 NC1 domains. J Biol Chem 2002, 277:40075-40083
3. Timpl R, Wiedemann H, van Delden V, Furthmayr H, Kuhn KA: Network model for the organization of type IV collagen molecules in basement membranes. Eur J Biochem 1981, 120:203-211
4. Yurchenco PD, Furthmayr H: Self-assembly of basement membrane collagen. Biochemistry 1984, 23:1839-1850
5. Gunwar S, Ballester F, Noelken ME, Sado Y, Ninomiya Y, Hudson BG: Glomerular basement membrane. Identification of a novel disulfide-cross-linked network of alpha3, alpha4, and alpha5 chains of type IV collagen and its implications for the pathogenesis of Alport syndrome. J Biol Chem 1998, 273:8767-8775
6. Kleppel MM, Santi PA, Cameron JD, Wieslander J, Michael AF: Human tissue distribution of novel basement membrane collagen. Am J Pathol 1989, 134:813-825
7. Butkowski R J, Wieslander J, Kleppel M, Michael AF, Fish AJ: Basement membrane collagen in the kidney: regional localization of novel chains related to collagen IV. Kidney Int 1989, 35:1195-1202
8. Hellmark T, Segelmark M, Wieslander J: Anti-GBM antibodies in Goodpasture syndrome; anatomy of an epitope. Nephrol Dial Transplant 1997, 12:646-648
9. Borza DB, Hudson BG: Molecular characterization of the target antigens of anti-GBM antibody disease. Springer Semin Immunopathol 2003, 4:345-361
10. Gubler MC, Antignac C, Deschênes G, Knebelmann B, Hors-Cayla MC, Grunfeld JP, Broyer M, Habib R: Genetic, clinical, and morphologic heterogeneity in Alport's syndrome. Adv Nephrol 1993, 22:15-35
11. Kalluri R, Shield CF, Todd P, Hudson BG, Neilson EG: Isoform switching of type IV collagen is developmentally arrested in X-linked Alport syndrome leading to increased susceptibility of renal basement membranes to endopreteolysis. J Clin Invest 1997, 99:2470-2478
12. Thorner PS, Zheng K, Kalluri R, Jacobs R, Hudson BG: Coordinate gene expression of the alpha3, alpha4, and alpha5 chains of collagen type IV Evidence from a canine model of X-linked nephritis with a COL4A5 gene mutation. J Biol Chem 1996, 271:13821-13828
13. Nakanishi K, Yoskikawa N, Iijima K, Nakamura H: Expression of type IV collagen alpha 3 and alpha 4 chain mRNA in X-linked Alport syndrome. J Am Soc Nephrol 1996, 7:938-945
14. Heidet L, Cai Y, Guicharnaud L, Antignac C, Gubler MC: Glomerular expression of type IV collagen chains in normal and X-linked Alport syndrome kidneys. Am J Pathol 2000, 156:1901-1910
15. Miner JH, Lewis RM, Sanes JR: Molecular and functional defects in kidney of mice lacking collagen α3(IV): implications for Alport syndrome. J Cell Biol 1996, 135:1403-1413
16. Cosgrove D, Meehan DT, Grunkemeyer JA, Kornak JM, Sayers R, Hunter WJ, Samuelson GC: Collagen COL4A3 knock out: a mouse model for autosomal Alport syndrome. Genes Dev 1996, 10:2981-2992
17. Boye E, Mollet G, Forestier L, Cohen-Solal L, Heidet L, Cochat P, Grünfeld JP, Palcoux JB, Gubler MC, Antignac C: Determination of the genomic structure of the COL4A4 gene and of novel mutations causing autosomal recessive Alport syndrome. Am J Hum Genet 1998, 63:1329-1340
18. Cohen D, Chumakov I, Weissenbach J: A first-generation physical map of the human genome. Nature 1993, 366:698-701
19. Heidet L, Cohen Solal L, Boye E, Thorner P, Kemper M, David A, Larget Piet L, Zhou J, Flinter F, Xu Z, Gubler MC, Antignac C: Novel COL4A5-COL4A6 deletion in diffuse leiomyomatosis-Alport syndrome (DL-AS) locus define the DL critical region. Cytogenet Cell Genet 1997, 78:240-246
20. Schedl A, Ross A, Lee M, Engelkamp D, Rashbass P, van Heyningen V, Hastie ND: Influence of PAX6 gene dosage on development: overexpression causes severe eye abnormalities. Cell 1996, 86:71-82
21. Barton MC, Hoekstra MF, Emerson BM: Site-directed, recombination-mediated mutagenesis of a complex gene locus. Nucleic Acids Res 1990, 18:7349-7355
22. Heidet L, Arrondel C, Forestier L, Cohen Solal L, Mollet G, Guttierrez B, Stavrou C, Gubler MC, Antignac C. Structure of the human type IV collagen gene COL4A3 and mutations in autosomal Alport syndrome. J Am Soc Nephrol 2001, 12:97-106
23. Schedl A, Larin Z, Montoliu L, Thies E, Kelsey G, Lehrach H, Schutz G: A method for the generation of YAC transgenic mice by pronuclear microinjection. Nucleic Acids Res 1993, 21:4783-4787
24. Matsuda Y, Harada YN, Natsuume-Sakai S, Lee K, Shiomi T, Chapman VM: Location of the mouse complement factor H gene (cfh) by FISH analysis and replication R-banding. Cytogenet Cell Genet 1992, 61:282-285
25. Lemieux N, Dutrillaux B, Viegas-Péquignot E: A simple method for simultaneous R- or G-banding and fluorescence in situ hybridization of small single-copy genes. Cytogenet Cell Genet 1992, 59:311-312
26. Sado Y, Kagawa M, Kishiro Y, Sugihara K, Naito I, Seyer JM, Sugimoto M, Oohashi T, Ninomiya Y: Establishment by the rat lymph node method of epitope-defined monoclonal antibodies recognizing the six different alpha chains of human type IV collagen. Histochem Cell Biol 1995, 104:267-275
27. Wieslander J: The Goodpasture antigen. Contrib Nephrol 1990, 80:56-67
28. Kagawa M, Kishiro Y, Naito I, Nemoto T, Nakanishi H, Ninomiya Y, Sado Y: Epitope-defined monoclonal antibodies against type-IV collagen for diagnosis of Alport's syndrome. Nephrol Dial Transplant 1997, 12:1238-1241
29. Kleppel MM, Fan WW, Cheong HI, Kashtan CE, Michael AF: Immunochemical studies of the Alport antigen. Kidney Int 1992, 41:1629-1637
30. Borza DB, Netzer KO, Leinonen A, Todd P, Cervera J, Saus J, Hudson BG: The Goodpasture autoantigen. Identification of multiple cryptic epitopes on the NC1 domain of the alpha3(IV) collagen chain. J Biol Chem 2000, 275:6030-6037
31. Cherqui S, Sevin C, Hamard G, Kalatzis V, Sich M, Pequignot MO, Gogat K, Abitbol M, Broyer M, Gubler MCG, Antignac C: Intralysosomal cystine accumulation in mice lacking cystinosin, the protein defective in cystinosis. Mol Cell Biol 2002, 22:7622-7632
32. Borza DB, Bondar O, Ninomiya Y, Sado Y, Naito I, Todd P, Hudson BG: The NC1 domain of collagen IV encodes a novel network composed of the alpha 1, alpha 2, alpha 5, and alpha 6 chains in smooth muscle basement membranes. J Biol Chem 2001, 276:28532-28540
33. Miner JH, Sanes J: Collagen IV α3, α4 and α5 chains in rodent basal laminae: sequence, distribution, association with laminins and developmental switches. J Cell Biol 1994, 127:879-891
34. Cosgrove D, Rodgers K, Meehan D, Miller C, Bovard K, Gilroy A, Gardner H, Kotelianski V, Gotwals P, Amatucci A, Kalluri R: Integrin alpha1 beta1 and transforming growth factor-beta1 play distinct roles in Alport glomerular pathogenesis and serve as dual targets for metabolic therapy. Am J Pathol 2000, 157:1649-1659
35. Kashtan CE, Kim Y, Lees GE, Thorner PS, Virtanen I, Miner JH: Abnormal glomerular basement membrane laminins in murine, canine, and human Alport syndrome: aberrant laminin alpha2 deposition is species independent. J Am Soc Nephrol 2001, 12:252-260
36. Seki T, Naito I, Oohashi T, Sado Y, Ninomiya Y: Differential expression of type IV collagen isoforms, alpha5(IV) and alpha6(IV) chains, in basement membranes surrounding smooth muscle cells. Histochem Cell Biol 1998, 110:359-366
37. Saito K, Naito I, Seki T, Oohashi T, Kimura E, Momota R, Kishiro Y, Sado Y, Yoshioka H, Ninomiya Y: Differential expression of mouse alpha5(IV) and alpha6(IV) collagen genes in epithelial basement membranes. J Biochem 2000, 128:427-434
38. Saus J, Wieslander J, Langeveld JP, Quinones S, Hudson BG: Identification of the Goodpasture antigen as the alpha 3(IV) chain of collagen IV. J Biol Chem 1988, 263:13374-13380
39. Heikkila P, Tibell A, Morita T, Chen Y, Wu G, Sado Y, Ninomiya Y, Petterson E. Tryggvason K: Adenovirus-mediated transfer of type IV collagen α5 chain c-DNA into swine kidney in vivo: deposition of the protein into the glomerular basement membrane. Gene Therapy 2001, 8:882-890
40. Bernal D, Quinones S, Saus J: The human mRNA encoding the Goodpasture antigen is alternatively spliced. J Biol Chem 1993, 268:12090-12094
41. Feng L, Xia Y, Wilson CB: Alternative splicing of the NC1 domain of the human alpha 3(IV) collagen gene. Differential expression of mRNA transcripts that predict three protein variants with distinct carboxyl regions. J Biol Chem 1994, 269:2342-2348
42. Heikkila P, Soininen R, Tryggvason K: Directional regulatory activity of cis-acting elements in the bi-directional alpha 1(IV) and alpha 2(IV) collagen gene promoter. J Biol Chem 1993, 268:24677-24682
43. Haniel A, Welge-Lussen U, Kuhn K, Poschl E: Identification and characterization of a novel transcriptional silencer in the human collagen type IV gene COL4A2. J Biol Chem 1995, 270:11209-11215
44. Sayers R, Kalluri R, Rodgers KD, Shield CF, Meehan DT, Cosgrove D: Role for transforming growth factor-beta1 in Alport renal disease progression. Kidney Int 1999, 56:1662-1673
45. Netzer KO, Leinonen A, Boutaud A, Borza DB, Todd P, Gunwar S, Langeveld JP, Hudson BG: The Goodpasture autoantigen. Mapping the major conformational epitope(s) of alpha3(IV) collagen to residues 17-31 and 127-141 of the NC1 domain. J Biol Chem 1999, 274:11267-11274
46. Cosgrove D, Gray D, Dierich A, Kaufman J, Lemeur M, Benoist C, Mathis D: Mice lacking MHC class II molecules. Cell 1991, 66:1051-1066
47. Meyers KE, Allen J, Gehret J, Jacobovits A, Gallo M, Neilson EG, Hopfer H, Kalluri R, Madaio MP: Human antiglomerular basement membrane autoantibody disease in XenoMouse 11. Kidney Int 2002, 61:1666-1673