Situs inversus and ciliary abnormalities: 20 years later, what is the connection?



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Situs inversus and ciliary abnormalities: 20 years later, what is the connection?

Petra Pennekamp1#, Tabea Menchen1, Bernd Dworniczak2, Hiroshi Hamada3


Supplementary Tables
Supplementary table 1: Genes that have been shown to influence ciliogenesis at the node in mice, ranging from complete absence to short or abnormal cilia.


Gene

full name

References

Acvr1

activin A receptor, type 1

[1,2]

Arl13b

ADP-ribosylation factor-like 13B

[3,4]

Atmin

ATM interactor

[5]

B9d1

B9 protein domain 1

[6]

B9d2

B9 protein domain 2

[6,7]

Cluap1

clusterin associated protein 1

[8]

Foxj1

forkhead box J1

[9,10]

Ift57

intraflagellar transport 57

[11]

Ift88

intraflagellar transport 88

[12,13]

Ift122

intraflagellar transport 122

[14]

Ift172

intraflagellar transport 172

[15,16]

Intu

inturned planar cell polarity effector homolog (Drosophila)

[17]

Kif3a

kinesin family member 3A

[18,19]

Kif3b

kinesin family member 3B

[20]

Mks1

Meckel syndrome, type 1

[21]

Noto

notochord homolog (Xenopus laevis)

[22]

Ofd1

oral-facial-digital syndrome 1 gene homolog (human)

[23]

Pifo

primary cilia formation

[24]

Rfx3

regulatory factor X, 3 (influences HLA class II expression)

[25]

Rpgrip1

Rpgrip1-like

[26]

T

brachyury

[27]

Talpid3

RIKEN cDNA 2700049A03 gene

[28-30]

Tbx6

T-box 6

[31]

Zic2

zinc finger protein of the cerebellum 2

[32]

Supplementary table 2: Genes that have been shown to influence node morphology and shape including orientation of cilia (PCP) which is necessary to generate directed leftward flow in mice.

Gene

full name

References

Bicc1

bicaudal C homolog 1 (Drosophila)

[33,34]

Dll1

delta-like 1 (Drosophila)

[35,36]

Dvl1 Dvl2 Dvl3

dishevelled, dsh homolog 1 (Drosophila) dishevelled 2, dsh homolog (Drosophila) dishevelled 3, dsh homolog (Drosophila)

[37]

Cfl1 + Vangl 2

cofilin 1, non-muscle + vang-like 2 (van gogh, Drosophila)

[38]

Ednrb

endothelin receptor type B

[39]

Epb4.1l5

erythrocyte protein band 4.1-like 5

[40]

Fn1

fibronectin 1

[41]

Foxa2

forkhead box A2

[42,43]

Invs

inversin

[44,45]

Notch1 + Notch2

notch 1 + notch2

[35]

Smarcd3

SWI/SNF related, matrix associated, actin dependent regulator of chromatin, subfamily d, member 3

[46]

Sufu

suppressor of fused homolog (Drosophila)

[47]

Vangl1+Vangl2

vang-like 1 (van gogh, Drosophila) +

vang-like 2 (van gogh, Drosophila)



[38]

Supplementary table 3: Genes that have been shown to cause axonemal defects resulting in dyskinetic cilia and PCD in with or without heterotaxy in humans (and mice).

Genes encoding subunits of axonemal outer dynein arm components

Gene

full name

References

DNAH5/Dnah5

dynein, axonemal, heavy chain 5

[48-51]

DNAH11/Dnah11

dynein, axonemal, heavy chain 11

[51-53]

DANI1/Dnaic1

dynein, axonemal, intermediate chain 1

[51,54-56]

DNAI2

dynein, axonemal, intermediate chain 2

[57]

DNAL1

dynein, axonemal, light chain 1

[58]

NME8

NME/NM23 family member 8

[59]




Genes encoding for proteins required for the docking of ODA complexes

Gene

full name

References

ARMC4/Armc4

armadillo repeat containing 4

[51,60]

CCDC114

coiled-coil domain containing 114

[61]

CCDC151/Ccdc151

coiled-coil domain containing 151

[62]




Genes encoding for proteins required for pre-assembly of dynein arm components

Gene

full name

References

C21ORF59

RIKEN cDNA 1110004E09 gene (human homolog: Chomosome 21 open reading frame 59)

[63]

CCDC103

coiled-coil domain containing 103

[64]

DNAAF1

dynein, axonemal assembly factor 1

[65]

DNAAF2/Dnaaf2

dynein, axonemal assembly factor 2

[66,67]

DNAAF3/Dnaaf3

dynein, axonemal assembly factor 3

[51,68]

DYX1C1/Dyx1c1

dyslexia susceptibility 1 candidate 1

[51,69]

HEATR2

HEAT repeat containing 2

[70]

LLRC6

leucine rich repeat containing 6

[71]

SPAG1

sperm associated antigen 1

[72]

ZMYND10

zinc finger, MYND-type containing 10

[73]




Genes influencing IDAs and nexin-dynein regulatory complexes (N-DRCs) and microtubular organization

Gene

full name

References

CCDC39

coiled-coil domain containing 39

[51,74]

CCDC40

coiled-coil domain containing 40

[75]




Genes encoding for N-DRC components *

Gene

full name

References

CCDC65

coiled-coil domain containing 65

[63]

DRC1/Drc1

dynein regulatory complex subunit 1

[51,76]

*For CCDC65 and DRC1/Drc1 so far no human laterality defects have been reported. But, for Drc1 a mouse mutant was identified by the Bench to Bassinet Program (B2B/CVDC) showing situs inversus totalis (Drc1b2b2237Clo [51]) suggesting that these genes are also important for cilia motility at the node.


Supplementary table 4: Genes that have been shown to cause PCD or RGMC. Laterality defects have not been observed so far in humans and mouse mutants.

Genes encoding for radial spoke proteins

Gene

full name

References

RSPH1/Rsph1

radial spoke head 1 homolog (Chlamydomonas)

[77-79]

RSPH4

radial spoke head 4 homolog (Chlamydomonas)

[78,80]

RSPH9

radial spoke head 9 homolog (Chlamydomonas)

[78-80]




Gene encoding for central pair complex components

Gene

full name

References

HYDIN/Hydin*

HYDIN, axonemal central pair apparatus protein

[81-83]




Genes causing reduced generation of multiple motile cilia (RGMC)

Gene

full name

References

CCNO

cyclin O

[84]

MCIDAS

multiciliate differentiation and DNA synthesis associated cell cycle protein

[85]


*HYDIN/Hydin encodes for a subunit of the central pair complex [82,83]. Lack of expression at the node and lack of laterality defects in these mutants provide high evidence that central pairs are not relevant for ciliary function during LR-development despite that fact that central pairs can be observed in nodal monocilia [86] (Figure 2).

Supplementary References


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