Katana VentraIP

p53 upregulated modulator of apoptosis

The p53 upregulated modulator of apoptosis (PUMA) also known as Bcl-2-binding component 3 (BBC3), is a pro-apoptotic protein, member of the Bcl-2 protein family.[5][6] In humans, the Bcl-2-binding component 3 protein is encoded by the BBC3 gene.[5][6] The expression of PUMA is regulated by the tumor suppressor p53. PUMA is involved in p53-dependent and -independent apoptosis induced by a variety of signals, and is regulated by transcription factors, not by post-translational modifications. After activation, PUMA interacts with antiapoptotic Bcl-2 family members, thus freeing Bax and/or Bak which are then able to signal apoptosis to the mitochondria. Following mitochondrial dysfunction, the caspase cascade is activated ultimately leading to cell death.[7]

Structure[edit]

The PUMA protein is part of the BH3-only subgroup of Bcl-2 family proteins. This group of proteins only share sequence similarity in the BH3 domain, which is required for interactions with Bcl-2-like proteins, such as Bcl-2 and Bcl-xL.[5] Structural analysis has shown that PUMA directly binds to antiapoptotic Bcl-2 family proteins via an amphiphatic α-helical structure which is formed by the BH3 domain.[8] The mitochondrial localization of PUMA is dictated by a hydrophobic domain on its C-terminal portion.[9] PUMA protein degradation is regulated by phosphorylation at a conserved serine residue at position 10.[31]

Mechanism of action[edit]

Biochemical studies have shown that PUMA interacts with antiapoptotic Bcl-2 family members such as Bcl-xL, Bcl-2, Mcl-1,[10] Bcl-w, and A1, inhibiting their interaction with the proapoptotic molecules, Bax and Bak. When the inhibition of these is lifted, they result in the translocation of Bax and activation of mitochondrial dysfunction resulting in release of mitochondrial apoptogenic proteins cytochrome c, SMAC, and apoptosis-inducing factor (AIF) leading to caspase activation and cell death.[5]


Because PUMA has high affinity for binding to Bcl-2 family members, another hypothesis is that PUMA directly activates Bax and/or Bak and through Bax multimerization triggers mitochondrial translocation and with it induces apoptosis.[11][12] Various studies have shown though, that PUMA does not rely on direct interaction with Bax/Bak to induce apoptosis.[13][14]

Regulation[edit]

Induction[edit]

The majority of PUMA induced apoptosis occurs through activation of the tumor suppressor protein p53. p53 is activated by survival signals such as glucose deprivation[15] and increases expression levels of PUMA. This increase in PUMA levels induces apoptosis through mitochondrial dysfunction. p53, and with it PUMA, is activated due to DNA damage caused by a variety of genotoxic agents. Other agents that induce p53 dependent apoptosis are neurotoxins,[16][17] proteasome inhibitors,[18] microtubule poisons,[19] and transcription inhibitors.[20] PUMA apoptosis may also be induced independently of p53 activation by other stimuli, such as oncogenic stress[21][22] growth factor and/or cytokine withdrawal and kinase inhibition,[6][23][24] ER stress, altered redox status,[25][26] ischemia,[11][27] immune modulation,[28][29] and infection.[7][30]

Degradation[edit]

PUMA levels are downregulated through the activation of caspase-3 and a protease inhibited by the serpase inhibitor N-tosyl-L-phenylalanine chloromethyl ketone, in response to signals such as the cytokine TGFβ, the death effector TRAIL or chemical drugs such as anisomycin.[31] PUMA protein is degraded in a proteasome dependent manner and its degradation is regulated by phosphorylation at a conserved serine residue at position 10.[32]

Role in cancer[edit]

Several studies have shown that PUMA function is affected or absent in cancer cells. Additionally, many human tumors contain p53 mutations,[33] which results in no induction of PUMA, even after DNA damage induced through irradiation or chemotherapy drugs.[34] Other cancers, which exhibit overexpression of antiapoptotic Bcl-2 family proteins, counteract and overpower PUMA-induced apoptosis.[35] Even though PUMA function is compromised in most cancer cells, it does not appear that genetic inactivation of PUMA is a direct target of cancer.[36][37][38] Many cancers do exhibit p53 gene mutations, making gene therapies that target this gene impossible, but an alternate pathway may be to focus on therapeutic to target PUMA and induce apoptosis in cancer cells. Animal studies have shown that PUMA does play a role in tumor suppression, but lack of PUMA activity alone does not translate to spontaneous formation of malignancies.[39][40][41][42][43] Inhibiting PUMA induced apoptosis may be an interesting target for reducing the side effects of cancer treatments, such as chemotherapy, which induce apoptosis in rapidly dividing healthy cells in addition to rapidly dividing cancer cells.[7]


PUMA can also function as an indicator of p53 mutations. Many cancers exhibit mutations in the p53 gene, but this mutation can only be detected through extensive DNA sequencing. Studies have shown that cells with p53 mutations have significantly lower levels of PUMA, making it a good candidate for a protein marker of p53 mutations, providing a simpler method for testing for p53 mutations.[44]

Apoptosis

Apoptosome

Bcl-2

(BAX)

Bcl-2-associated X protein

(BID)

BH3 interacting domain death agonist

Caspases

Cytochrome c

Noxa

Mitochondrion

Overview of all the structural information available in the for UniProt: Q9BXH1 (Human Bcl-2-binding component 3, isoforms 1/2) at the PDBe-KB.

PDB

Overview of all the structural information available in the for UniProt: Q99ML1 (Mouse Bcl-2-binding component 3) at the PDBe-KB.

PDB