Differential cadherin expression in the developing postnatal telencephalon of a new world monkey

Journal of Comparative Neurology

Volumn 521, Issue 17, 2013, Pages 4027-4060

  Matsunaga, Eiji ^a   Nambu, Sanae ^a   Oka, Mariko ^a   Iriki, Atsushi ^a  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Cadherin; Evolution; Gene expression; Marmoset; Mouse; Telencephalon

Indexed keywords

CADHERIN; CADHERIN 10; CADHERIN 11; CADHERIN 12; CADHERIN 20; CADHERIN 4; CADHERIN 6; CADHERIN 7; CADHERIN 8; CADHERIN 9; GLYCOPROTEIN; T CADHERIN; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN CORTEX; BRAIN DEVELOPMENT; CALLITRICHINAE; CONTROLLED STUDY; DENTATE GYRUS; ENTORHINAL CORTEX; FEMALE; GLOBUS PALLIDUS; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SUBICULUM; TELENCEPHALON;

CADHERIN; EVOLUTION; GENE EXPRESSION; MARMOSET; MOUSE; TELENCEPHALON;

ANIMALS; ANIMALS, NEWBORN; CADHERINS; CALLITHRIX; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; PLATYRRHINI; TELENCEPHALON;

EID: 84885446686     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23389     Document Type: Article

References (72)

1. Arndt K, Redies C. 1996. Restricted expression of R-cadherin by brain nuclei and neural circuits of the developing chicken brain. J Comp Neurol 373:373-399.
2. Arndt K, Redies C. 1998. Development of cadherin-defined parasagittal subdivisions in the embryonic chicken cerebellum. J Comp Neurol 401:367-381.
3. Barnes SH, Price SR, Wentzel C, Guthrie SC. 2010. Cadherin-7 and cadherin-6B differentially regulate the growth, branching and guidance of cranial motor axons. Development 137:805-814.
4. Bekirov IH, Needleman LA, Zhang W, Benson DL. 2002. Identification and localization of multiple classic cadherins in developing rat limbic system. Neuroscience 115:213-227.
5. Bourne JA, Warner CE, Rosa MG. 2005. Topographic and laminar maturation of striate cortex in early postnatal marmoset monkeys, as revealed by neurofilament immunohistochemistry. Cereb Cortex 15:740-748.
6. Bozdagi O, Shan W, Tanaka H, Benson DL, Huntley GW. 2000. Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 28:245-259.
7. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, Kodzius R, Shimokawa K, Bajic VB, Brenner SE, Batalov S, Forrest AR, Zavolan M, Davis MJ, Wilming LG, Aidinis V, Allen JE, Ambesi-Impiombato A, Apweiler R, Aturaliya RN, Bailey TL, Bansal M, Baxter L, Beisel KW, Bersano T, Bono H, Chalk AM, Chiu KP, Choudhary V, Christoffels A, Clutterbuck DR, Crowe ML, Dalla E, Dalrymple BP, de Bono B, Della Gatta G, di Bernardo D, Down T, Engstrom P, Fagiolini M, Faulkner G, Fletcher CF, Fukushima T, Furuno M, Futaki S, Gariboldi M, Georgii-Hemming P, Gingeras TR, Gojobori T, Green RE, Gustincich S, Harbers M, Hayashi Y, Hensch TK, Hirokawa N, Hill D, Huminiecki L, Iacono M, Ikeo K, Iwama A, Ishikawa T, Jakt M, Kanapin A, Katoh M, Kawasawa Y, Kelso J, Kitamura H, Kitano H, Kollias G, Krishnan SP, Kruger A, Kummerfeld SK, Kurochkin IV, Lareau LF, Lazarevic D, Lipovich L, Liu J, Liuni S, McWilliam S, Madan Babu M, Madera M, Marchionni L, Matsuda H, Matsuzawa S, Miki H, Mignone F, Miyake S, Morris K, Mottagui-Tabar S, Mulder N, Nakano N, Nakauchi H, Ng P, Nilsson R, Nishiguchi S, Nishikawa S, Nori F, Ohara O, Okazaki Y, Orlando V, Pang KC, Pavan WJ, Pavesi G, Pesole G, Petrovsky N, Piazza S, Reed J, Reid JF, Ring BZ, Ringwald M, Rost B, Ruan Y, Salzberg SL, Sandelin A, Schneider C, Schönbach C, Sekiguchi K, Semple CA, Seno S, Sessa L, Sheng Y, Shibata Y, Shimada H, Shimada K, Silva D, Sinclair B, Sperling S, Stupka E, Sugiura K, Sultana R, Takenaka Y, Taki K, Tammoja K, Tan SL, Tang S, Taylor MS, Tegner J, Teichmann SA, Ueda HR, van Nimwegen E, Verardo R, Wei CL, Yagi K, Yamanishi H, Zabarovsky E, Zhu S, Zimmer A, Hide W, Bult C, Grimmond SM, Teasdale RD, Liu ET, Brusic V, Quackenbush J, Wahlestedt C, Mattick JS, Hume DA, Kai C, Sasaki D, Tomaru Y, Fukuda S, Kanamori-Katayama M, Suzuki M, Aoki J, Arakawa T, Iida J, Imamura K, Itoh M, Kato T, Kawaji H, Kawagashira N, Kawashima T, Kojima M, Kondo S, Konno H, Nakano K, Ninomiya N, Nishio T, Okada M, Plessy C, Shibata K, Shiraki T, Suzuki S, Tagami M, Waki K, Watahiki A, Okamura-Oho Y, Suzuki H, Kawai J, Hayashizaki Y; FANTOM Consortium; RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group). 2005. The transcriptional landscape of the mammalian genome. Science 309:1559-1563.
8. Etzrodt J, Krishna-K K, Redies C. 2009. Expression of classic cadherins and delta-protocadherins in the developing ferret retina. BMC Neurosci 10:153.
9. Fushimi D, Arndt K, Takeichi M, Redies C. 1997. Cloning and expression analysis of cadherin-10 in the CNS of the chicken embryo. Dev Dyn 209:269-285.
10. Hatta K, Takeichi M. 1986. Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature 320:447-449.
11. Hertel N, Krishna-K, Nuernberger M, Redies C. 2008. A cadherin-based code for the divisions of the mouse basal ganglia. J Comp Neurol 508:511-528.
12. Hertel N, Redies C, Medina L. 2012. Cadherin expression delineates the divisions of the postnatal and adult mouse amygdala. J Comp Neurol 520:3982-4012.
13. Hirano S, Takeichi M. 2012. Cadherins in brain morphogenesis and wiring. Physiol Rev 92:597-634.
14. Hulpiau P, van Roy F. 2011. New insights into the evolution of metazoan cadherins. Mol Biol Evol 28:647-657.
15. Inoue T, Tanaka T, Suzuki SC, Takeichi M. 1998. Cadherin-6 in the developing mouse brain: expression along restricted connection systems and synaptic localization suggest a potential role in neuronal circuitry. Dev Dyn 211:338-351.
16. Inoue T, Tanaka T, Takeichi M, Chisaka O, Nakamura S, Osumi N. 2001. Role of cadherins in maintaining the compartment boundary between the cortex and striatum during development. Development 128:561-569.
17. Johnson MB, Kawasawa YI, Mason CE, Krsnik Z, Coppola G, Bogdanovič D, Geschwind DH, Mane SM, State MW, Sestan N. 2009. Functional and evolutionary insights into human brain development through global transcriptome analysis. Neuron 62:494-509.
18. Jones EG, Rubenstein JL. 2004. Expression of regulatory genes during differentiation of thalamic nuclei in mouse and monkey. J Comp Neurol 477:55-80.
19. Ju MJ, Aroca P, Luo J, Puelles L, Redies C. 2004. Molecular profiling indicates avian branchiomotor nuclei invade the hindbrain alar plate. Neuroscience 128:785-796.
20. Kadowaki M, Nakamura S, Machon O, Krauss S, Radice GL, Takeichi M. 2007. N-cadherin mediates cortical organization in the mouse brain. Dev Biol 304:22-33.
21. Kim SY, Chung HS, Sun W, Kim H. 2007. Spatiotemporal expression pattern of non-clustered protocadherin family members in the developing rat brain. Neuroscience 147:996-1021.
22. Kim SY, Mo JW, Han S, Choi SY, Han SB, Moon BH, Rhyu IJ, Sun W, Kim H. 2009. The expression of non-clustered protocadherins in adult rat hippocampal formation and the connecting brain regions. Neuroscience 170:189-199.
23. Korematsu K, Redies C. 1997. Restricted expression of cadherin-8 in segmental and functional subdivisions of the embryonic mouse brain. Dev Dyn 208:178-189.
24. Krishna-K, Nuernberger M, Weth F, Redies C. 2009. Layer-specific expression of multiple cadherins in the developing visual cortex (V1) of the ferret. Cereb Cortex 19:388-401.
25. Krishna-K, Hertel N, Redies C. 2011. Cadherin expression in the somatosensory cortex: evidence for a combinatorial molecular code at the single-cell level. Neuroscience 175:37-48.
26. Lefkovics K, Mayer M, Bercsényi K, Szabó G, Lele Z. 2012. Comparative analysis of type II classic cadherin mRNA distribution patterns in the developing and adult mouse somatosensory cortex and hippocampus suggests significant functional redundancy. J Comp Neurol 520:1387-1405.
27. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH, Kuan CL, Lake JH, Laramee AR, Larsen KD, Lau C, Lemon TA, Liang AJ, Liu Y, Luong LT, Michaels J, Morgan JJ, Morgan RJ, Mortrud MT, Mosqueda NF, Ng LL, Ng R, Orta GJ, Overly CC, Pak TH, Parry SE, Pathak SD, Pearson OC, Puchalski RB, Riley ZL, Rockett HR, Rowland SA, Royall JJ, Ruiz MJ, Sarno NR, Schaffnit K, Shapovalova NV, Sivisay T, Slaughterbeck CR, Smith SC, Smith KA, Smith BI, Sodt AJ, Stewart NN, Stumpf KR, Sunkin SM, Sutram M, Tam A, Teemer CD, Thaller C, Thompson CL, Varnam LR, Visel A, Whitlock RM, Wohnoutka PE, Wolkey CK, Wong VY, Wood M, Yaylaoglu MB, Young RC, Youngstrom BL, Yuan XF, Zhang B, Zwingman TA, Jones AR. 2006. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168-176.
28. Lin J, Luo J, Redies C. 2008. Molecular cloning and expression analysis of three cadherin-8 isoforms in the embryonic chicken brain. Brain Res 1201:1-14.
29. Manabe T, Togashi H, Uchida N, Suzuki SC, Hayakawa Y, Yamamoto M, Yoda H, Miyakawa T, Takeichi M, Chisaka O. 2000. Loss of cadherin-11 adhesion receptor enhances plastic changes in hippocampal synapses and modifies behavioral responses. Mol Cell Neurosci 15:534-546.
30. Mashiko H, Yoshida AC, Kikuchi SS, Niimi K, Takahashi E, Aruga J, Okano H, Shimogori T. 2012. Comparative anatomy of marmoset and mouse cortex from genomic expression. J Neurosci 32:5039-5053.
31. Matsunaga E, Okanoya K. 2008. Expression analysis of cadherins in the songbird brain: relationship to vocal system evolution. J Comp Neurol 508:329-342.
32. Matsunaga E, Okanoya K. 2011. Comparative gene expression analysis among vocal learners (Bengalese finch and budgerigar) and non-learners (quail and ring dove) reveals variable cadherin expressions in the vocal system. Front Neuroanat 5:28.
33. Matsunaga E, Nambu S, Iriki A, Okanoya K. 2011a. Expression pattern of cadherins in the naked mole rat (Heterocephalus glaber) suggests innate cortical diversification of the cerebrum. J Comp Neurol 519:1736-1747.
34. Matsunaga E, Suzuki K, Kato S, Kurotani T, Kobayashi K, Okanoya K. 2011b. Dynamic expression of cadherins regulates vocal development in a songbird. PLoS ONE 6:e25272.
35. Matsunaga E, Kurotani T, Suzuki K, Okanoya K. 2011c. Type-II cadherins modulate neural activity in cultured rat hippocampal neurons. Neuroreport 22:629-632.
36. Matsunaga E, Nambu S, Oka M, Okanoya K, Iriki A. 2013. Comparative analysis of protocadherin-11 X-linked expression among postnatal rodents, non-human primates, and songbirds suggests its possible involvement in brain evolution. PLoS ONE 8:e58840.
37. Mayer M, Bercsényi K, Géczi K, Szabó G, Lele Z. 2010. Expression of two type II cadherins, Cdh12 and Cdh22 in the developing and adult mouse brain. Gene Expr Patterns 10:351-360.
38. Nakagawa S, Takeichi M. 1995. Neural crest cell-cell adhesion controlled by sequential and subpopulation-specific expression of novel cadherins. Development 121:1321-1332.
39. Nakagawa S, Takeichi M. 1998. Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 125:2963-2971.
40. Nakagawa R, Matsunaga E, Okanoya K. 2012. Defects in ultrasonic vocalization of cadherin-6 knockout mice. PLoS ONE 7:e49233.
41. Neudert F, Nuernberger KK, Redies C. 2008. Comparative analysis of cadherin expression and connectivity patterns in the cerebellar system of ferret and mouse. J Comp Neurol 511:736-752.
42. Ohno S. 1999. Gene duplication and the uniqueness of vertebrate genomes circa 1970-1999. Semin Cell Dev Biol 10:517-522.
43. Osterhout JA, Josten N, Yamada J, Pan F, Wu SW, et al. 2011. Cadherin-6 mediates axon-target matching in a non-image-forming visual circuit. Neuron 71:632-639.
44. Pagnamenta AT, Khan H, Walker S, Gerrelli D, Wing K, Bonaglia MC, Giorda R, Berney T, Mani E, Molteni M, Pinto D, Le Couteur A, Hallmayer J, Sutcliffe JS, Szatmari P, Paterson AD, Scherer SW, Vieland VJ, Monaco AP. 2011. Rare familial 16q21 microdeletions under a linkage peak implicate cadherin 8 (CDH8) in susceptibility to autism and learning disability. J Med Genet 48:48-54.
45. Pistorio AL, Vintch B, Wang X. 2006. Acoustic analysis of vocal development in a New World primate, the common marmoset (Callithrix jacchus). J Acoust Soc Am 120:1655-1670.
46. Price SR, De Marco Garcia NV, Ranscht B, Jessell TM. 2002. Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109:205-216.
47. Rakic P. 1974. Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183:425-427.
48. Redies C, Takeichi M. 1996. Cadherins in the developing central nervous system: an adhesive code for segmental and functional subdivisions. Dev Biol 180:413-423.
49. Redies C, Ast M, Nakagawa S, Takeichi M, Martínez-de-la-Torre M, Puelles L. 2000. Morphologic fate of diencephalic prosomeres and their subdivisions revealed by mapping cadherin expression. J Comp Neurol 421:481-514.
50. Redies C, Medina L, Puelles L. 2001. Cadherin expression by embryonic divisions and derived gray matter structures in the telencephalon of the chicken. J Comp Neurol 438:253-285.
51. Redies C, Vanhalst K, Roy F. 2005. Delta-protocadherins: unique structures and functions. Cell Mol Life Sci 62:2840-2852.
52. Redies C, Hertel N, Hübner CA. 2012. Cadherins and neuropsychiatric disorders. Brain Res 1470:130-144.
53. Saarimäki-Vire J, Alitalo A, Partanen J. 2011. Analysis of Cdh22 expression and function in the developing mouse brain. Dev Dyn 240:1989-2001.
54. Sasaki E, Suemizu H, Shimada A, Hanazawa K, Oiwa R, Kamioka M, Tomioka I, Sotomaru Y, Hirakawa R, Eto T, Shiozawa S, Maeda T, Ito M, Ito R, Kito C, Yagihashi C, Kawai K, Miyoshi H, Tanioka Y, Tamaoki N, Habu S, Okano H, Nomura T. Nature. 2009. Generation of transgenic non-human primates with germline transmission. Nature 459:523-527.
55. Shimoyama Y, Tsujimoto G, Kitajima M, Natori M. 2000. Identification of three human type II classic cadherins and frequent heterophilic interactions between different subclasses of type II classic cadherins. Biochem J 349:159-167.
56. Suzuki SC, Takeichi M. 2008. Cadherins in neuronal morphogenesis and function. Dev Growth Differ 50(Suppl 1):S119-S130.
57. Suzuki SC, Inoue T, Kimura Y, Tanaka T, Takeichi M. 1997. Neuronal circuits are subdivided by differential expression of type II classic cadherins in postnatal mouse brains. Mol Cell Neurosci 9:433-447.
58. Suzuki SC, Furue H, Koga K, Jiang N, Nohmi M, Shimazaki Y, Katoh-Fukui Y, Yokoyama M, Yoshimura M, Takeichi M. 2007. Cadherin-8 is required for the first relay synapses to receive functional inputs from primary sensory afferents for cold sensation. J Neurosci 27:3466-3476.
59. Takahashi M, Osumi N. 2005. Identification of a novel type II classical cadherin: rat cadherin19 is expressed in the cranial ganglia and Schwann cell precursors during development. Dev Dyn 232:200-208.
60. Takahashi M, Osumi N. 2008. Expression study of cadherin7 and cadherin20 in the embryonic and adult rat central nervous system. BMC Dev Biol 19:87.
61. Takeichi M. 1995. Morphogenetic roles of classic cadherins. Curr Opin Cell Biol 7:619-627.
62. Takeichi M. 2007. The cadherin superfamily in neuronal connections and interactions. Nat Rev Neurosci 8:11-20.
63. Togashi H, Abe K, Mizoguchi A, Takaoka K, Chisaka O, Takeichi M. 2002. Cadherin regulates dendritic spine morphogenesis. Neuron 35:77-89.
64. Treubert-Zimmermann U, Heyers D, Redies C. 2002. Targeting axons to specific fiber tracts in vivo by altering cadherin expression. J Neurosci 22:7617-7626.
65. Vanhalst K, Kools P, Staes K, van Roy F, Redies C. 2005. Delta-protocadherins: a gene family expressed differentially in the mouse brain. Cell Mol Life Sci 62:1247-1259.
66. Wheelock MJ, Shintani Y, Maeda M, Fukumoto Y, Johnson KR. 2008. Cadherin switching. J Cell Sci 121:727-735.
67. Williams ME, Wilke SA, Daggett A, Davis E, Otto S, et al. 2011. Cadherin-9 regulates synapse-specific differentiation in the developing hippocampus. Neuron 71:640-655.
68. Wöhrn JC, Puelles L, Nakagawa S, Takeichi M, Redies C. 1998. Cadherin expression in the retina and retinofugal pathways of the chicken embryo. J Comp Neurol 396:20-38.
69. Wöhrn JC, Nakagawa S, Ast M, Takeichi M, Redies C. 1999. Combinatorial expression of cadherins in the tectum and the sorting of neurites in the tectofugal pathways of the chicken embryo. Neuroscience 90:985-1000.
70. Yagi T. 2008. Clustered protocadherin family. Dev Growth Differ 50(Suppl 1):S131-S140.
71. Yamazaki Y, Echigo C, Saiki M, Inada M, Watanabe S, Iriki A. 2011. Tool-use learning by common marmosets (Callithrix jacchus). Exp Brain Res 213:63-71.
72. Yoon MS, Puelles L, Redies C. 2000. Formation of cadherin-expressing brain nuclei in diencephalic alar plate divisions. J Comp Neurol 427:461-480.