Insights into the early evolution of animal calcium signaling machinery: A unicellular point of view

Cell Calcium

Volumn 57, Issue 3, 2015, Pages 166-173

  Cai, Xinjiang ^a   Wang, Xiangbing ^a   Patel, Sandip ^b   Clapham, David E ^c,d  

^a ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Animals; Calcium channels; Calcium signaling; Choanoflagellates; Evolution; Genomics

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; SODIUM CALCIUM EXCHANGE PROTEIN; SPERM SPECIFIC VOLTAGE GATED CALCIUM CHANNEL BETA; SPERM SPECIFIC VOLTAGE GATED CALCIUM CHANNEL DELTA; SPERM SPECIFIC VOLTAGE GATED CALCIUM CHANNEL GAMMA; TRANSIENT RECEPTOR POTENTIAL CHANNEL; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

AMOEBOZOA; ANIMAL GENETICS; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE PERMEABILITY; CELLULAR DISTRIBUTION; CHANNEL GATING; CHOANOFLAGELLATE; CILIARY MOTILITY; COMPARATIVE STUDY; COMPLEX FORMATION; CYTOSOL; ENDOPLASMIC RETICULUM; EUKARYOTE EVOLUTION; EVOLUTIONARY HOMOLOGY; FILASTEREA; FUNGUS; GENETIC CONSERVATION; GENETIC VARIABILITY; GENOMICS; MAMMAL; MAMMAL CELL; MOLECULAR EVOLUTION; NONHUMAN; OPISTHOKONTA; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROKARYOTE; PROTIST; REVIEW; SARCOPLASMIC RETICULUM; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS; THECAMONAS TRAHENS; ANIMAL; EUKARYOTE; EVOLUTION; METABOLISM; PHYLOGENY; PHYSIOLOGY; PLANT;

ANIMALIA; CHOANOFLAGELLIDA; EUKARYOTA; FUNGI; PROKARYOTA;

ANIMALS; BIOLOGICAL EVOLUTION; CALCIUM SIGNALING; EUKARYOTA; FUNGI; PHYLOGENY; PLANTS;

EID: 84924080589     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2014.11.007     Document Type: Review

References (105)

1. Clapham D.E. Calcium signaling. Cell 2007, 131:1047-1058.
2. Dominguez D.C. Calcium signalling in bacteria. Mol. Microbiol. 2004, 54:291-297.
3. Verret F., Wheeler G., Taylor A.R., Farnham G., Brownlee C. Calcium channels in photosynthetic eukaryotes: implications for evolution of calcium-based signalling. New Phytol. 2010, 187:23-43.
4. Kudla J., Batistic O., Hashimoto K. Calcium signals: the lead currency of plant information processing. Plant Cell 2010, 22:541-563.
5. Zelter A., Bencina M., Bowman B.J., Yarden O., Read N.D. A comparative genomic analysis of the calcium signaling machinery in Neurospora crassa, Magnaporthe grisea, and Saccharomyces cerevisiae. Fungal Genet. Biol. 2004, 41:827-841.
6. Berridge M.J., Bootman M.D., Roderick H.L. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 2003, 4:517-529.
7. Case R.M., Eisner D., Gurney A., Jones O., Muallem S., Verkhratsky A. Evolution of calcium homeostasis: from birth of the first cell to an omnipresent signalling system. Cell Calcium 2007, 42:345-350.
8. Kazmierczak J., Kempe S., Kremer B. Calcium in the early evolution of living systems: a biohistorical approach. Curr. Org. Chem. 2013, 17:1738-1750.
9. Verkhratsky A., Parpura V. Calcium signalling and calcium channels: evolution and general principles. Eur. J. Pharmacol. 2014, 739C:1-3.
10. 2+ signaling. Trends Cell Biol. 2010, 20:277-286.
11. 2+ influx in human sperm. Nature 2011, 471:382-386.
12. 2+ channel of human sperm. Nature 2011, 471:387-391.
13. Rokas A. The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu. Rev. Genet. 2008, 42:235-251.
14. Richter D.J., King N. The genomic and cellular foundations of animal origins. Annu. Rev. Genet. 2013, 47:509-537.
15. Nagata T., Iizumi S., Satoh K., et al. Comparative analysis of plant and animal calcium signal transduction element using plant full-length cDNA data. Mol. Biol. Evol. 2004, 21:1855-1870.
16. McAinsh M.R., Pittman J.K. Shaping the calcium signature. New Phytol. 2009, 181:275-294.
17. Bell G., Mooers A.O. Size and complexity among multicellular organisms. Biol. J. Linn. Soc. 1997, 60:345-363.
18. Rokas A. The molecular origins of multicellular transitions. Curr. Opin. Genet. Dev. 2008, 18:472-478.
19. 2+ exchanger superfamily: phylogenetic analysis and structural implications. Mol. Biol. Evol. 2004, 21:1692-1703.
20. Nagamune K., Sibley L.D. Comparative genomic and phylogenetic analyses of calcium ATPases and calcium-regulated proteins in the apicomplexa. Mol. Biol. Evol. 2006, 23:1613-1627.
21. 2+ signaling 'toolkit' at the origin of metazoa. Mol. Biol. Evol. 2008, 25:1357-1361.
22. 2+ signalling in plants and green algae - changing channels. Trends Plant Sci. 2008, 13:506-514.
23. 2+ signaling machinery in early animal and fungal evolution. Mol. Biol. Evol. 2012, 29:91-100.
24. 2+ signalling early in evolution - all but primitive. J. Cell Sci. 2013, 126:2141-2150.
25. 2+ signaling machinery: conservation of the CatSper channel complex. Mol. Biol. Evol. 2014, 31:2735-2740.
26. Edel K.H., Kudla J. Increasing complexity and versatility: How the calcium signaling toolkit was shaped during plant land colonization. Cell Calcium 2015, 57:231-246.
27. Stechmann A., Cavalier-Smith T. Rooting the eukaryote tree by using a derived gene fusion. Science 2002, 297:89-91.
28. Richards T.A., Cavalier-Smith T. Myosin domain evolution and the primary divergence of eukaryotes. Nature 2005, 436:1113-1118.
29. Derelle R., Lang B.F. Rooting the eukaryotic tree with mitochondrial and bacterial proteins. Mol. Biol. Evol. 2012, 29:1277-1289.
30. Srivastava M., Simakov O., Chapman J., et al. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 2010, 466:720-726.
31. Sakarya O., Armstrong K.A., Adamska M., et al. A post-synaptic scaffold at the origin of the animal kingdom. PLoS ONE 2007, 2:e506.
32. Knoll A.H. The multiple origins of complex multicellularity. Annu. Rev. Earth Planet. Sci. 2011, 39:217-239.
33. King N., Westbrook M.J., Young S.L., et al. The genome of the choanoflagellate Monosiga brevicollis and the origins of metazoan multicellularity. Nature 2008, 451:783-788.
34. King N. Choanoflagellates. Curr. Biol. 2005, 15:R113-R114.
35. Lang B.F., O'Kelly C., Nerad T., Gray M.W., Burger G. The closest unicellular relatives of animals. Curr. Biol. 2002, 12:1773-1778.
36. Steenkamp E.T., Wright J., Baldauf S.L. The protistan origins of animals and fungi. Mol. Biol. Evol. 2006, 23:93-106.
37. Ruiz-Trillo I., Roger A.J., Burger G., Gray M.W., Lang B.F. A phylogenomic investigation into the origin of metazoa. Mol. Biol. Evol. 2008, 25:664-672.
38. Suga H., Chen Z., de Mendoza A., et al. The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat. Commun. 2013, 4:2325.
39. Sebe-Pedros A., de Mendoza A., Lang B.F., Degnan B.M., Ruiz-Trillo I. Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol. Biol. Evol. 2011, 28:1241-1254.
40. Fairclough S.R., Chen Z., Kramer E., et al. Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol. 2013, 14:R15.
41. Dayel M.J., Alegado R.A., Fairclough S.R., et al. Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Dev. Biol. 2011, 357:73-82.
42. Sebe-Pedros A., Irimia M., Del Campo J., et al. Regulated aggregative multicellularity in a close unicellular relative of metazoa. Elife 2013, 2:e01287.
43. Cavalier-Smith T., Chao E.E. Phylogeny and evolution of apusomonadida (protozoa: apusozoa): new genera and species. Protist 2010, 161:549-576.
44. Ruiz-Trillo I., Burger G., Holland P.W., et al. The origins of multicellularity: a multi-taxon genome initiative. Trends Genet. 2007, 23:113-118.
45. Sebe-Pedros A., Roger A.J., Lang F.B., King N., Ruiz-Trillo I. Ancient origin of the integrin-mediated adhesion and signaling machinery. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:10142-10147.
46. Burki F., Pawlowski J. Monophyly of Rhizaria and multigene phylogeny of unicellular bikonts. Mol. Biol. Evol. 2006, 23:1922-1930.
47. Chan C.X., Reyes-Prieto A., Bhattacharya D. Red and green algal origin of diatom membrane transporters: insights into environmental adaptation and cell evolution. PLoS ONE 2011, 6:e29138.
48. Plattner H. Calcium regulation in the protozoan model, Paramecium tetraurelia. J. Eukaryot. Microbiol. 2014, 61:95-114.
49. Valentine J.W., Collins A.G., Meyer C.P. Morphological complexity increase in metazoans. Paleobiology 1994, 20:131-142.
50. Parekh A.B., Putney J.W. Store-operated calcium channels. Physiol. Rev. 2005, 85:757-810.
51. Philipson K.D., Nicoll D.A. Sodium-calcium exchange: a molecular perspective. Annu. Rev. Physiol. 2000, 62:111-133.
52. Wu L.J., Sweet T.B., Clapham D.E. International Union of Basic and Clinical Pharmacology. LXXVI. Current progress in the mammalian TRP ion channel family. Pharmacol. Rev. 2010, 62:381-404.
53. 2+ signaling. Cold Spring Harb. Perspect. Biol. 2010, 2:a003962.
54. 2+ channel subunit, Orai. J. Mol. Biol. 2007, 368:1284-1291.
55. 2+ entry: stromal interaction molecule. PLoS ONE 2007, 2:e609.
56. 2+ signaling systems. Trends Cell Biol. 2011, 21:202-211.
57. Klauke N., Blanchard M., Plattner H. Polyamine triggering of exocytosis in Paramecium involves an extracellular Ca(2+)/(polyvalent cation)-sensing receptor, subplasmalemmal Ca-store mobilization and store-operated Ca(2+)-influx via unspecific cation channels. J. Membr. Biol. 2000, 174:141-156.
58. 2+ influx in Paramecium. J. Membr. Biol. 2002, 187:1-14.
59. 2+ release channels participate in the secretory cycle of Paramecium cells. Mol. Cell. Biol. 2009, 29:3605-3622.
60. Yu X., Duan K.L., Shang C.F., Yu H.G., Zhou Z. Calcium influx through hyperpolarization-activated cation channels (I(h) channels) contributes to activity-evoked neuronal secretion. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:1051-1056.
61. Cai X. Evolutionary genomics reveals the premetazoan origin of opposite gating polarity in animal-type voltage-gated ion channels. Genomics 2012, 99:241-245.
62. Cai X. P2X receptor homologs in basal fungi. Purinergic Signal. 2012, 8:11-13.
63. Fountain S.J., Burnstock G. An evolutionary history of P2X receptors. Purinergic Signal. 2009, 5:269-272.
64. Amador F.J., Stathopulos P.B., Enomoto M., Ikura M. Ryanodine receptor calcium release channels: lessons from structure-function studies. FEBS J. 2013, 280:5456-5470.
65. Ladenburger E.M., Korn I., Kasielke N., Wassmer T., Plattner H. An Ins(1,4,5)P3 receptor in Paramecium is associated with the osmoregulatory system. J. Cell Sci. 2006, 119:3705-3717.
66. Ladenburger E.M., Plattner H. Calcium-release channels in Paramecium. Genomic expansion, differential positioning and partial transcriptional elimination. PLoS ONE 2011, 6:e27111.
67. Plattner H. Calcium signalling in the ciliated protozoan model, Paramecium: strict signal localisation by epigenetically controlled positioning of different Ca-channels. Cell Calcium 2014, [Epub ahead of print]. 10.1016/j.ceca.2014.09.003.
68. Mackrill J.J. Ryanodine receptor calcium release channels: an evolutionary perspective. Adv. Exp. Med. Biol. 2012, 740:159-182.
69. + channels predates the divergence of animals and fungi. J. Membr. Biol. 2012, 245:117-123.
70. Liebeskind B.J., Hillis D.M., Zakon H.H. Evolution of sodium channels predates the origin of nervous systems in animals. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:9154-9159.
71. Cheng X., Shen D., Samie M., Xu H. Mucolipins intracellular TRPML1-3 channels. FEBS Lett. 2010, 584:2013-2021.
72. Brailoiu E., Churamani D., Cai X., et al. Essential requirement for two-pore channel 1 in NAADP-mediated calcium signaling. J. Cell Biol. 2009, 186:201-209.
73. Bick A.G., Calvo S.E., Mootha V.K. Evolutionary diversity of the mitochondrial calcium uniporter. Science 2012, 336:886.
74. Mitchell D.R. The evolution of eukaryotic cilia and flagella as motile and sensory organelles. Adv. Exp. Med. Biol. 2007, 607:130-140.
75. Ren D., Navarro B., Perez G., et al. A sperm ion channel required for sperm motility and male fertility. Nature 2001, 413:603-609.
76. DeCaen P.G., Delling M., Vien T.N., Clapham D.E. Direct recording and molecular identification of the calcium channel of primary cilia. Nature 2013, 504:315-318.
77. Delling M., DeCaen P.G., Doerner J.F., Febvay S., Clapham D.E. Primary cilia are specialized calcium signalling organelles. Nature 2013, 504:311-314.
78. Lishko P.V., Kirichok Y., Ren D., Navarro B., Chung J.J., Clapham D.E. The control of male fertility by spermatozoan ion channels. Annu. Rev. Physiol. 2012, 74:453-475.
79. Cai X., Clapham D.E. Evolutionary genomics reveals lineage-specific gene loss and rapid evolution of a sperm-specific ion channel complex: CatSpers and CatSperβ. PLoS ONE 2008, 3:e3569.
80. Pommerville J.C., Strickland J.B., Harding K.E. Pheromone interactions and ionic communication in gametes of aquatic fungus Allomyces macrogynus. J. Chem. Ecol. 1990, 16:121-131.
81. Riisberg I., Orr R.J., Kluge R., et al. Seven gene phylogeny of heterokonts. Protist 2009, 160:191-204.
82. Price D.C., Chan C.X., Yoon H.S., et al. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 2012, 335:843-847.
83. Qi H., Moran M.M., Navarro B., et al. All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:1219-1223.
84. Chung J.J., Navarro B., Krapivinsky G., Krapivinsky L., Clapham D.E. A novel gene required for male fertility and functional CATSPER channel formation in spermatozoa. Nat. Commun. 2011, 2:153.
85. Liman E.R., Innan H. Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:3328-3332.
86. Cai X., Patel S. Degeneration of an intracellular ion channel in the primate lineage by relaxation of selective constraints. Mol. Biol. Evol. 2010, 27:2352-2359.
87. 2+ exchanger, NCKX2. J. Biol. Chem. 2002, 277:48923-48930.
88. 2+ exchanger, NCX1. J. Mol. Cell. Cardiol. 2013, 57:68-71.
89. Liao J., Li H., Zeng W., Sauer D.B., Belmares R., Jiang Y. Structural insight into the ion-exchange mechanism of the sodium/calcium exchanger. Science 2012, 335:686-690.
90. Waight A.B., Pedersen B.P., Schlessinger A., et al. Structural basis for alternating access of a eukaryotic calcium/proton exchanger. Nature 2013, 499:107-110.
91. Shigaki T., Rees I., Nakhleh L., Hirschi K.D. Identification of three distinct phylogenetic groups of CAX cation/proton antiporters. J. Mol. Evol. 2006, 63:815-825.
92. 2+/cation antiporters and insights into their evolution in plants. Front. Plant Sci. 2012, 3:1.
93. Clapham D.E., Garbers D.L. International Union of Pharmacology. L. Nomenclature and structure-function relationships of CatSper and two-pore channels. Pharmacol. Rev. 2005, 57:451-454.
94. 2+ exchanger from an archaebacterium. J. Biol. Chem. 2012, 287:8652-8659.
95. Fujinami S., Terahara N., Krulwich T.A., Ito M. Motility and chemotaxis in alkaliphilic Bacillus species. Future Microbiol. 2009, 4:1137-1149.
96. Liebeskind B.J., Hillis D.M., Zakon H.H. Independent acquisition of sodium selectivity in bacterial and animal sodium channels. Curr. Biol. 2013, 23:R948-R949.
97. Armstrong C.M., Hille B. Voltage-gated ion channels and electrical excitability. Neuron 1998, 20:371-380.
98. Strong M., Chandy K.G., Gutman G.A. Molecular evolution of voltage-sensitive ion channel genes: on the origins of electrical excitability. Mol. Biol. Evol. 1993, 10:221-242.
99. Payandeh J., Scheuer T., Zheng N., Catterall W.A. The crystal structure of a voltage-gated sodium channel. Nature 2011, 475:353-358.
100. Zhang X., Ren W., DeCaen P., et al. Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature 2012, 486:130-134.
101. Yue L., Navarro B., Ren D., Ramos A., Clapham D.E. The cation selectivity filter of the bacterial sodium channel, NaChBac. J. Gen. Physiol. 2002, 120:845-853.
102. Heinemann S.H., Terlau H., Stuhmer W., Imoto K., Numa S. Calcium channel characteristics conferred on the sodium channel by single mutations. Nature 1992, 356:441-443.
103. 2+ channels. Nature 1993, 366:158-161.
104. + channels. Sci. Signal. 2014, 7:ra109.
105. Liebeskind B.J., Hillis D.M., Zakon H.H. Phylogeny unites animal sodium leak channels with fungal calcium channels in an ancient, voltage-insensitive clade. Mol. Biol. Evol. 2012, 29:3613-3616.