Old genes and new genes: The evolution of the kallikrein locus

Summary

The human kallikrein locus consists of KLK1, the gene of major tissue kallikrein, and 14 genes of kallikrein-related peptidases (KLKs) located in tandem on chromosome 19q13.3-13.4. In this review, based on information retrieved from the literature or extracted from genome databases, it is hypothesised that the kallikrein locus is unique to mammals. The majority of genes are highly conserved, as demonstrated by the identification of 11 KLK genes in the opossum, a metatherian species. In contrast, a sublocus, encompassing KLK1-4, has gone through major transformations that have generated new genes, which in most cases are closely related to KLK1. In the primate lineage, this process created KLK3, the gene of the prostate cancer marker, prostate-specific antigen (PSA), whereas in the murine lineage it gave rise to 13 genes unique to the mouse and nine unique to the rat. The KLK proteases are effector molecules that emerged early in mammalian evolution and their importance in skin homeostasis and male reproductive function is undisputed and there are also accumulating evidence for a role of KLK proteases in the development of the brain. It is speculated that the KLK gene family arose as part of the process that generated distinguishing mammalian features, like skin with hair and sweat glands, and specialised anatomical attributes of the brain and the reproductive tract.

Keywords

Serine peptidase - gene family - conservation - duplication - PSA

• References

• 1 Gan L, Lee I, Smith R. et al. Sequencing and expression analysis of the serine protease gene cluster located in chromosome 19q13 region. Gene 2000; 257: 119-130.
• 2 Harvey TJ, Hooper JD, Myers SA. et al. Tissue-specific expression patterns and fine mapping of the human kallikrein (KLK) locus on proximal 19q13.4. J Biol Chem 2000; 275: 37397-37406.
• 3 Yousef GM, Chang A, Scorilas A. et al. Genomic organization of the human kallikrein gene family on chromosome 19q13.3-q13.4. Biochem Biophys Res Commun 2000; 276: 125-133.
• 4 Olsson AY, Lilja H, Lundwall A. Taxon-specific evolution of glandular kallikrein genes and identification of a progenitor of prostate-specific antigen. Genomics 2004; 84: 147-156.
• 5 Olsson AY, Lundwall A. Organization and evolution of the glandular kallikrein locus in Mus musculus. Biochem Biophys Res Commun 2002; 299: 305-311.
• 6 Elliott MB, Irwin DM, Diamandis EP. In silico identification and Bayesian phylogenetic analysis of multiple new mammalian kallikrein gene families. Genomics 2006; 88: 591-599.
• 7 Olsson AY, Valtonen-Andre C, Lilja H. et al. The evolution of the glandular kallikrein locus: identification of orthologs and pseudogenes in the cotton-top tamarin. Gene 2004; 343: 347-355.
• 8 Pavlopoulou A, Pampalakis G, Michalopoulos I. et al. Evolutionary history of tissue kallikreins. PLoS One 2010; 05: e13781.
• 9 Lundwall Å. Evolution of kallikrein-related peptidases. In: Kallikrein-related peptidases, Vol 1,Characterization, regulation, and interactions within the protease web. De Gruyter 2012; pp. 79-96.
• 10 Murphy WJ, Eizirik E, Johnson WE. et al. Molecular phylogenetics and the origins of placental mammals. Nature 2001; 409: 614-618.
• 11 Waddell PJ, Kishino H, Ota R. A phylogenetic foundation for comparative mammalian genomics. Genome Inform 2001; 12: 141-154.
• 12 Hallstrom BM, Kullberg M, Nilsson MA. et al. Phylogenomic data analyses provide evidence that Xenarthra and Afrotheria are sister groups. Mol Biol Evol 2007; 24: 2059-2068.
• 13 Song S, Liu L, Edwards SV. et al. Resolving conflict in eutherian mammal phylogeny using phylogenomics and the multispecies coalescent model. Proc Natl Acad Sci USA 2012; 109: 14942-14947.
• 14 Fry BG. From genome to "venome": molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins. Genome Res 2005; 15: 403-420.
• 15 Fry BG, Vidal N, Norman JA. et al. Early evolution of the venom system in lizards and snakes. Nature 2006; 439: 584-588.
• 16 Lundwall A, Brattsand M. Kallikrein-related peptidases. Cell Mol Life Sci 2008; 65: 2019-2038.
• 17 Schedlich LJ, Bennetts BH, Morris BJ. Primary structure of a human glandular kallikrein gene. DNA 1987; 06: 429-437.
• 18 Lundwall A, Lilja H. Molecular cloning of human prostate specific antigen cDNA. FEBS Lett 1987; 214: 317-322.
• 19 Kaushal A, Myers SA, Dong Y. et al. A novel transcript from the KLKP1 gene is androgen regulated, down-regulated during prostate cancer progression and encodes the first non-serine protease identified from the human kallikrein gene locus. Prostate 2008; 68: 381-399.
• 20 Lu W, Zhou D, Glusman G. et al. KLK31P is a novel androgen regulated and transcribed pseudogene of kallikreins that is expressed at lower levels in prostate cancer cells than in normal prostate cells. Prostate 2006; 66: 936-944.
• 21 Yousef GM, Borgono CA, Michael IP. et al. Cloning of a kallikrein pseudogene. Clin Biochem 2004; 37: 961-967.
• 22 Malm J, Hellman J, Hogg P. et al. Enzymatic action of prostate-specific antigen (PSA or hK3): substrate specificity and regulation by Zn(2+), a tight-binding inhibitor. Prostate 2000; 45: 132-139.
• 23 Robert M, Gibbs BF, Jacobson E. et al. Characterization of prostate-specific antigen proteolytic activity on its major physiological substrate, the sperm motility inhibitor precursor/semenogelin I. Biochemistry 1997; 36: 3811-3819.
• 24 Bode W, Chen Z, Bartels K. et al. Refined 2 A X-ray crystal structure of porcine pancreatic kallikrein A, a specific trypsin-like serine proteinase. Crystallization, structure determination, crystallographic Refinement, structure and its comparison with bovine trypsin. J Mol Biol 1983; 164: 237-382.
• 25 Lovgren J, Airas K, Lilja H. Enzymatic action of human glandular kallikrein 2 (hK2). Substrate specificity and regulation by Zn2+ and extracellular protease inhibitors. Eur J Biochem 1999; 262: 781-789.
• 26 Chapdelaine P, Dube JY, Frenette G. et al. Identification of arginine esterase as the major androgen-dependent protein secreted by dog prostate and preliminary molecular characterization in seminal plasma. J Androl 1984; 05: 206-210.
• 27 Lazure C, Leduc R, Seidah NG. et al. The major androgen-dependent protease in dog prostate belongs to the kallikrein family: confirmation by partial amino acid sequencing. FEBS Lett 1984; 175: 1-7.
• 28 Carvalho AL, Sanz L, Barettino D. et al. Crystal structure of a prostate kallikrein isolated from stallion seminal plasma: a homologue of human PSA. J Mol Biol 2002; 322: 325-337.
• 29 Ashley PL, MacDonald RJ. Kallikrein-related mRNAs of the rat submaxillary gland: nucleotide sequences of four distinct types including tonin. Biochemistry 1985; 24: 4512-4520.
• 30 Mason AJ, Evans BA, Cox DR. et al. Structure of mouse kallikrein gene family suggests a role in specific processing of biologically active peptides. Nature 1983; 303: 300-307.
• 31 Fukushima D, Kitamura N, Nakanishi S. Nucleotide sequence of cloned cDNA for human pancreatic kallikrein. Biochemistry 1985; 24: 8037-8043.
• 32 Lundwall A. Characterization of the gene for prostate-specific antigen, a human glandular kallikrein. Biochem Biophys Res Commun 1989; 161: 1151-1159.
• 33 Riegman PH, Vlietstra RJ, Klaassen P. et al. The prostate-specific antigen gene and the human glandular kallikrein-1 gene are tandemly located on chromosome 19. FEBS Lett 1989; 247: 123-126.
• 34 Riegman PH, Vlietstra RJ, van der Korput JA. et al. Characterization of the prostate-specific antigen gene: a novel human kallikrein-like gene. Biochem Biophys Res Commun 1989; 159: 95-102.
• 35 Evans BA, Drinkwater CC, Richards RI. Mouse glandular kallikrein genes. Structure and partial sequence analysis of the kallikrein gene locus. J Biol Chem 1987; 262: 8027-8034.
• 36 Frey P, Forand R, Maciag T. et al. The biosynthetic precursor of epidermal growth factor and the mechanism of its processing. Proc Natl Acad Sci USA 1979; 76: 6294-6298.
• 37 Berger EA, Shooter EM. Evidence for pro-beta-nerve growth factor, a biosynthetic precursor to beta-nerve growth factor. Proc Natl Acad Sci USA 1977; 74: 3647-3651.
• 38 Bothwell MA, Wilson WH, Shooter EM. The relationship between glandular kallikrein and growth factor-processing proteases of mouse submaxillary gland. J Biol Chem 1979; 254: 7287-7294.
• 39 Karn RC, Laukaitis CM. Positive selection shaped the convergent evolution of independently expanded kallikrein subfamilies expressed in mouse and rat saliva proteomes. PLoS One 2011; 06: e20979.
• 40 van Leeuwen BH, Penschow JD, Coghlan JP. et al. Cellular basis for the differential response of mouse kallikrein genes to hormonal induction. EMBO J 1987; 06: 1705-1713.
• 41 Wines DR, Brady JM, Pritchett DB. et al. Organization and expression of the rat kallikrein gene family. J Biol Chem 1989; 264: 7653-7662.
• 42 Southard-Smith M, Pierce JC, MacDonald RJ. Physical mapping of the rat tissue kallikrein family in two gene clusters by analysis of P1 bacteriophage clones. Genomics 1994; 22: 404-417.
• 43 MacDonald RJ, Southard-Smith EM, Kroon E. Disparate tissue-specific expression of members of the tissue kallikrein multigene family of the rat. J Biol Chem 1996; 271: 13684-13690.
• 44 Clements JA, Matheson BA, Wines DR. et al. Androgen dependence of specific kallikrein gene family members expressed in rat prostate. J Biol Chem 1988; 263: 16132-16137.
• 45 Wines DR, Brady JM, Southard EM. et al. Evolution of the rat kallikrein gene family: gene conversion leads to functional diversity. J Mol Evol 1991; 32: 476-492.
• 46 Lawrence MG, Lai J, Clements JA. Kallikreins on steroids: structure, function, and hormonal regulation of prostate-specific antigen and the extended kallikrein locus. Endocr Rev 2010; 31: 407-446.
• 47 Sotiropoulou G, Pampalakis G, Diamandis EP. Functional roles of human kallikrein-related peptidases. J Biol Chem 2009; 284: 32989-32994.
• 48 Shiosaka S, Ishikawa Y. Neuropsin--a possible modulator of synaptic plasticity. J Chem Neuroanat 2011; 42: 24-29.