Evolution of hematopoiesis: Three members of the PU.1 transcription factor family in a cartilaginous fish, Raja eglanteria - PubMed (original) (raw)

Comparative Study

. 2001 Jan 16;98(2):553-8.

doi: 10.1073/pnas.98.2.553. Epub 2001 Jan 9.

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Comparative Study

Evolution of hematopoiesis: Three members of the PU.1 transcription factor family in a cartilaginous fish, Raja eglanteria

M K Anderson et al. Proc Natl Acad Sci U S A. 2001.

Abstract

T lymphocytes and B lymphocytes are present in jawed vertebrates, including cartilaginous fishes, but not in jawless vertebrates or invertebrates. The origins of these lineages may be understood in terms of evolutionary changes in the structure and regulation of transcription factors that control lymphocyte development, such as PU.1. The identification and characterization of three members of the PU.1 family of transcription factors in a cartilaginous fish, Raja eglanteria, are described here. Two of these genes are orthologs of mammalian PU.1 and Spi-C, respectively, whereas the third gene, Spi-D, is a different family member. In addition, a PU.1-like gene has been identified in a jawless vertebrate, Petromyzon marinus (sea lamprey). Both DNA-binding and transactivation domains are highly conserved between mammalian and skate PU.1, in marked contrast to lamprey Spi, in which similarity is evident only in the DNA-binding domain. Phylogenetic analysis of sequence data suggests that the appearance of Spi-C may predate the divergence of the jawed and jawless vertebrates and that Spi-D arose before the divergence of the cartilaginous fish from the lineage leading to the mammals. The tissue-specific expression patterns of skate PU.1 and Spi-C suggest that these genes share regulatory as well as structural properties with their mammalian orthologs.

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Figures

Figure 1

Figure 1

Neighbor-joining tree of Ets DNA binding domain amino acid sequences of vertebrate PU.1 family transcription factors. This tree was constructed by using the

me tree

program, using proportions of differences as a distance measure and excluding gaps. This method finds a phylogenetic tree and statistically similar trees likely to represent a minimum total genetic difference (branch length) among the genes. The value at each node represents the probability that that branch length is not zero. GenBank accession nos.: mouse PU.1, L03215; human PU.1, X52056; chicken PU.1, Y12225; teleost fish PU.1, AF247366; X_enopus_ Spi-B, AF247365; caiman Spi-B, AF247364; human Spi-B, X66079; monkey Spi-B, AF025395; lamprey Spi, AF247362; mouse Spi-C, AF025395; fish Spi-C, AF247367; mouse GABPα, M74515; and mouse Elf-5, NM_010125.

Figure 2

Figure 2

Amino acid alignments of vertebrate PU.1 genes. The predicted amino acid sequence of skate PU.1 is aligned with PU.1 sequences from mouse, human, chicken, and teleost fish by using

clustalw

(see Fig. 1 legend for GenBank accession nos.). Stars indicate identity in all sequences, and dots indicate conserved types of amino acids. The transactivation domain is divided into four functionally relevant subdomains indicated above the sequence. The colored amino acids have been shown to be necessary for mouse PU.1 transactivation activity; Ser-148 is pink.

Figure 3

Figure 3

Amino acid alignment of jawed vertebrate PU.1 family members with lamprey Spi. This alignment was generated by using

clustalw

and includes the entire coding sequence of each gene. Boxes indicate known functional domains. Conserved types of amino acids are color-coded according to the

clustalx

program (32). See Fig. 1 legend for GenBank accession numbers.

Figure 4

Figure 4

Real-time reverse transcription–PCR analysis of PU.1 family member expression in adult skate tissues. Total RNA was random-primed to generate the cDNAs used as templates for SYBR green-based real-time PCRs. All results are normalized to levels of 28S rRNA.

Figure 5

Figure 5

Proposed scheme for evolution of vertebrate PU.1 family members. A common ancestor of the PU.1 family members was duplicated at least once before the emergence of the jawed vertebrates. In the lamprey, an N-terminal domain (yellow) containing a stretch of acidic residues (light yellow) and a stretch of glutamines (gray) was incorporated. In the jawed vertebrates, two different types of N-terminal regions evolved, neither of which is detectably related to the lamprey N-terminal region. The PU.1/Spi-D/Spi-B precursor (pink and purple N terminus) duplicated once, resulting in a PU.1/Spi-D precursor and a Spi-B type gene, followed by duplication of the PU.1/Spi-D precursor into two genes: PU.1 and Spi-D. These two duplications may have occurred between the emergence of the jawless and the jawed vertebrates. The other type of N-terminal domain (light blue) is associated with a significantly more divergent Ets domain (hatched dark blue), represented by Spi-C.

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