Expanding the lysyl hydroxylase toolbox: New insights into the localization and activities of Lysyl Hydroxylase 3 (LH3)

Journal of Cellular Physiology

Volumn 212, Issue 2, 2007, Pages 323-329

  Myllylä, Raili ^a   Wang, Chunguang ^a   Heikkinen, Jari ^a   Juffer, Andre ^a   Lampela, Outi ^a   Risteli, Maija ^a   Ruotsalainen, Heli ^a   Salo, Antti ^a   Sipilä, Laura ^a  

^a UNIVERSITY OF OULU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4; GLUCOSYLGALACTOSYLHYDROXYLYSINE; HYDROXYLYSINE; LYSYL HYDROXYLASE 3; PROCOLLAGEN GLUCOSYLTRANSFERASE; PROCOLLAGEN LYSINE 2 OXOGLUTARATE 5 DIOXYGENASE; UNCLASSIFIED DRUG;

BASEMENT MEMBRANE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENZYME ANALYSIS; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; LETHAL MUTANT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MODIFICATION; REVIEW; SEQUENCE ANALYSIS; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMALS; BASEMENT MEMBRANE; CATALYTIC DOMAIN; COLLAGEN; EMBRYONIC DEVELOPMENT; ENDOPLASMIC RETICULUM; EXTRACELLULAR SPACE; GALACTOSYLTRANSFERASES; GLUCOSYLTRANSFERASES; GLYCOSYLATION; HUMANS; HYDROXYLYSINE; MICE; MOLECULAR SEQUENCE DATA; PROCOLLAGEN-LYSINE, 2-OXOGLUTARATE 5-DIOXYGENASE; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY;

DANIO RERIO; MUS;

EID: 34347382592     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21036     Document Type: Review

References (55)

1. Armstrong LC, Last JA. 1995. Rat lysyl hydroxylase: Molecular cloning, mRNA distribution and expression in a baculovirus system. Biochim Biophys Acta 1264:93-102.
2. Bateman JF, Lamande SR, Ramshaw JAM. 1996. Collagen super-family. In: Comper WD, editors. Extracellular Matrix, Molecular Components and Interactions. Amsterdam: Harwood Academic Publishers. pp 22-67.
3. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer ELL, Studholme DJ, Yeats C, Eddy SR. 2004. The Pfam protein families database. Nucleic Acids Res 32:D138-D141. (Database issue).
4. Eyre DR, Wu JJ. 2005. Collagen cross-links. Top Curr Chem 247:207-229.
5. Franco OL, Rigden DJ. 2003. Fold recognition analysis of glycosyltransferase families: Further members of structural super-families. Glycobiology 13:707-712.
6. Franzke CW, Bruckner P, Bruckner-Tuderman L. 2005. Collagenous transmembrane proteins: Recent insights into biology and pathology. J Biol Chem 280:4005-4008.
7. Hautala T, Byers MG, Eddy RL, Shows TB, Kivirikko KI, Myllylä R. 1992a. Cloning of human lysyl hydroxylase: Complete cDNA-derived amino acid sequence and assignment of the gene (PLOD) to chromosome 1p36. 3-p36.2. Genomics 13:62-69.
8. Hautala T, Heikkinen J, Kivirikko KI, Myllylä R. 1992b. Minoxidil specifically decreases the expression of lysine hydroxylase in cultured human skin fibroblasts. Biochem J 283:51-54.
9. Heikkinen J, Hautala T, Kivirikko KI, Myllylä R. 1994. Structure and expression of human lysyl hydroxylase gene. Introns 9 and 16 contain Alu sequences at the sites of recombination in Ehlers-Danlos syndrome type VI patients. Genomics 24:464-471.
10. Heikkinen J, Risteli M, Wang C, Latvala J, Rossi M, Valtavaara M, Myllylä R. 2000. Lysyl hydroxylase 3 is a multifunctional protein possessing collagen glucosyltransferase activity. J Biol Chem 275:36158-36163.
11. Kadler K. 1994. Synthesis and degradation of collagen. Protein Profile 1:525-534, 545-549.
12. Kellokumpu S, Sormunen R, Heikkinen J, Myllylä R. 1994. Lysyl hydroxylase, a collagen processing enzyme, exemplifies a novel class of luminally-oriented peripheral membrane proteins in the endoplasmic reticulum. J Biol Chem 269:30524-30529.
13. Kielty CM, Hopkinson I, Grant ME. 1993. Collagen: The collagen family: Structure, assembly and organization in the extracellular matrix. In: Royce PM, Steinmann B, editors. Connective Tissue and Its Heritable Disorders. New York Wiley-Liss. pp 103-147.
14. Kivirikko KI, Myllylä R. 1979. Collagen glycosyltransferases. Int Rev Connect Tissue Res 8:23-72.
15. Kivirikko KI, Myllylä R. 1982. Post-translational enzymes in the biosynthesis of collagen: Intracellular enzymes. Methods Enzymol 82:245-304.
16. Kivirikko KI, Myllylä R, Pihlajaniemi T. 1992. Hydroxylation of proline and lysine residues in collagens and other animal and plant proteins. In: Harding JJ, Crabbe MJC, editors. Posttranslational Modifications of Proteins. Boca Raton: CRC Press. pp 1-51.
17. Kobayashi H, Ouchi N, Kihara S, Walsch K, Kumada M, Abe Y, Funahashi T, Matsuzawa Y. 2004. Selective suppression of endothelial cell apoptosis by the high molecular weight form of adiponectin. Circ Res 94:27-31.
18. Mercer DK, Nicol PF, Kimbembe C, Robins SP. 2003. Identification, expression and tissue distribution of the three rat lysyl hydroxylase isoforms. Biochem Biophys Res Commun 307:803-809.
19. Myllyharju J, Kivirikko KI. 2001. Collagens and collagen-related diseases. Ann Med 33:7-21.
20. Myllyharju J, Kivirikko KI. 2004. Collagens, modifyung enzymes and their mutations in humans, flies and worms. Trends Genet 20:33-43.
21. Myllylä R, Risteli L, Kivirikko KI. 1976. Collagen glucosyltransferase. Partial purification and characterization of the enzyme from whole chick embryos and chick embryo cartilage. Eur J Biochem 61:59-67.
22. Myllylä R, Pihlajaniemi T, Pajunen L, Turpeenniemi-Hujanen T, Kivirikko KI. 1991. Molecular cloning of chick lysyl hydroxylase. Little homology in primary structure to the two types of subunit of prolyl 4-hydroxylase. J Biol Chem 266:2805-2810.
23. Norman K, Moerman DG. 2000. The let-268 locus of Caenorhabditis elegans encodes a procollagen lysyl hydroxylase that is essential for type IV collagen secretion. Dev Biol 227:690-705.
24. Nowrocki AR, Rajala MW, Tomas E, Pajvani UB, Saha AK, Trumbauer ME, Pang Z, Chen AS, Ruderman NB, Chen H, Rossetti L, Scherer PE. 2006. Mice lacking adiponectin show decreased hepatic insulin sensitivity and reduced responsiveness to peroxisome proliferator-activated receptor gamma agonists. J Biol Chem 281:2654-2660.
25. Passoja K, Myllyharju J, Pirskanen A, Kivirikko KI. 1998a. Identification of arginine-700 as the residue that binds the C-5 carboxyl group of 2-oxoglutarate in human lysyl hydroxylase 1. FEBS Lett 434:145-148.
26. Passoja K, Rautavuoma K, Ala-Kokko L, Kosonen T, Kivirikko KI. 1998b. Cloning and characterization of a third human lysyl hydroxylase isoform. Proc Natl Acad Sci USA 95:10482-10486.
27. Pirskanen A, Kaimio AM, Myllylä R, Kivirikko KI. 1996. Site-directed mutagenesis of human lysyl hydroxylases expressed in insect cells. Identification of histidine residues and aspartic acid residue critical for catalytic activity. J Biol Chem 271:9398-9402.
28. Prockop DJ, Kivirikko KI. 1995. Collagens, molecular biology, diseases and potentials for gene therapy. Annu Rev Biochem 64:403-434.
29. Rautavuoma K, Passoja K, Helaakoski T, Kivirikko KI. 2000. Complete exon-intron organization of the gene for human lysyl hydroxylase 3 (LH3). Matrix Biol 19:73-79.
30. Rautavuoma K, Takaluoma K, Passoja K, Pirskanen A, Kvist AP, Kivirikko KI, Myllyharju J. 2002. Characterization of three fragments that constitute the monomers of the human lysyl hydroxylase isoenzymes 1, 2 and 3. The 30 kDa N-terminal fragment is not required for lysyl hydroxylase activity. J Biol Chem 277:23084-23091.
31. Rautavuoma K, Takaluoma K, Sormunen R, Myllyharju J, Kivirikko KI, Soininen R. 2004. Premature aggregation of type IV collagen and early lethality on lysyl hydroxylase 3 null mice. Proc Natl Acad Sci USA 101:14120-14125.
32. Richards AA, Stephens T, Charlton HK, Jones A, Macdonald GA, Prins JB, Whitehead JP. 2006. Adiponectin multimerization is dependent on conserved lysines in the collagenous domain: Evidence for regulation of multimerization by alterations in posttranslational modifications. Mol Endocrinol 20:1673-1687.
33. Risteli L, Myllylä R, Kivirikko KI. 1976. Affinity chromatography of collagen glycosyltransferases on collagen linked to agarose. Eur J Biochem 67:197-202.
34. Risteli M, Niemitalo O, Lankinen H, Juffer A, Myllylä R. 2004. Characterization of collagenous peptides bound to lysyl hydroxylase isoforms. J Biol Chem 279:37535-37543.
35. Robins SP, Brady JD. 2002. Collagen cross-linking and metabolism. In: Bilezikian JP, Raisz LG, Rodan GA, editors. Principles of Bone Biology. Vol. 1 . New York: Academic Press. pp 211-223.
36. Ruotsalainen H. 2005. Lysyl hydroxylases. Characterization of mouse lysyl hydroxylases and generation of genetically modified lysyl hydroxylase 3 mouse lines. Acta Universitatis Ouluensis A437 1-73. (Oulu University Press).
37. Ruotsalainen H, Sipilä L, Kerkelä R. Pospiech H, Myllylä R. 1999. Characterization of cDNAs for mouse lysyl hydroxylase 1,2 and 3, their phylogenetic analysis and tissue-specific expression in the mouse. Matrix Biol 18:325-329.
38. Ruotsalainen H, Vanhatupa S, Tampio M, Sipilä L, Valtavaara M, Myllylä R. 2001. Complete genomic structure of mouse lysyl hydroxylase 2 and lysyl hydroxylase 3/collagen glucosyltransferase. Matrix Biol 20:137-146.
39. Ruotsalainen H, Sipilä L, Vapola M, Sormunen R, Salo AM, Uitto L, Mercer DK, Robins SP, Risteli M, Attila A, Fässler R, Myllylä R. 2006. Glycosylation catalyzed by lysyl hydroxylase 3 (LH3) is essential for basement membranes. J Cell Sci 119:625-635.
40. Salo AM, Wang C, Sipilä L, Ruotsalainen H, Sormunen R, Vapola M, Kervinen P, Ruotsalainen H, Myllylä R. 2006a. Lysyl hydroxylase 3 (LH3) modifies proteins in the extracellular space, a novel mechanism for matrix remodelling. J Cell Physiol 207:644-653.
41. Salo AM, Sipilä L, Sormunen R, Ruotsalainen H, Vainio S, Myllylä R. 2006b. The lysyl hydroxylase isoforms are widely expressed during embryogenesis, but show tissue and cell specific regulation in the adult mouse. Matrix Biol 25:475-483.
42. Schneider VA, Granato M. 2006. The myotomal diwanka (Ih3) glycosyltransferase and type XVIII collagen are critical for motor growth cone migration. Neuron 50:683-695.
43. Schneider VA, Granato M. 2007. Genomic structure and embryonic expression of zebrafish lysyl hydroxylase 1 and lysyl hydroxylase 2. Matrix Biol 26:12-19.
44. Shi J, Blundell TL, Mizuguchi K. 2001. FUGUE: Sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol 310:243-257.
45. Sipilä L, Szatanik M, Vainionpää H, Ruotsalainen H, Myllylä R, Guénet JL. 2000. The genes encoding mouse lysyl hydroxylase isoforms map to Chromosomes 4,5,and 9. Mamm Genome 11:1132-1134.
46. Suokas M, Lampela O, Juffer A, Myllylä R, Kellokumpu S. 2003. Retrieval independent localization of lysyl hydroxylase in the endoplasmic reticulum via a peptide fold in its iron-binding domain. Biochem J 370:913-920.
47. Valtavaara M. 1999. Novel lysyl hydroxylase isoforms. Acta Univ Ouluensis A334:1-63.
48. Valtavaara M, Papponen H, Pirttilä AM, Hiltunen K, Helander H, Myllylä R. 1997. Cloning and characterization of a novel human lysyl hydroxylase isoform highly expressed in pancreas and muscle. J Biol Chem 272:6831-6834.
49. Valtavaara M, Szpirer C, Szpirer J, Myllylä R. 1998. Primary structure, tissue distribution and chromosomal localization of a novel isoform of lysyl hydroxylase (lysyl hydroxylase 3). J Biol Chem 273:12881-12886.
50. Valtavaara M, Szpirer C, Szpirer J, Myllylä R. 2000. Primary structure, tissue distribution and chromosomal localization of a novel isoform of lysyl hydroxylase (lysyl hydroxylase 3). J Biol Chem 275:20956.
51. Wang C, Valtavaara M, Myllylä R. 2000. Lack of collagen type specificity for lysyl hydroxylase isoforms. DNA Cell Biol 19:71-77.
52. Wang C, Luosujärvi H, Heikkinen J, Risteli M, Uitto L, Myllylä R. 2002a. The third activity for lysyl hydroxylase 3: Galactosylation of hydroxylysyl residues in collagens in vitro. Matrix Biol 21:559-566.
53. Wang C, Risteli M, Heikkinen J, Hussa AK, Uitto L, Myllylä R. 2002b. Identification of amino acids important for the catalytic activity of the collagen glucosyltransferase associated with the multifunctional lysyl hydroxylase 3 (LH3). J Biol Chem 277:18568-18573.
54. Wang Y, Lam KSL, Chan L, Chan KW, Lam JBB, Lam MC, Hoo RCL, Mak WWN, Cooper GJS, Xu A. 2006. Post-translational modifications of the four conserved lysine residues within the collagenous domain of adiponectin are required for the formation of its high molecular weight oligomeric complex. J Biol Chem 281:16391-16400.
55. Yeowell HN, Walker LC. 1999. Tissue specificity of a new splice form of the human lysyl hydroxylase 2 gene. Matrix Biol 18:179-187.